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MORPHOLOGY OF ANGIOSPERMS

VOIP i O OG
COE *2AINEG OES Ia

(MORPHOLOGY OF SPERMATOPHYTES. Part Il)

BY
JOHN MERLE COULTER, Pu. D.
HEAD OF DEPARTMENT OF BOTANY, THE UNIVERSITY OF CHICAGO

AND

CHARLES JOSEPH CHAMBERLAIN, Pu. D.

INSTRUCTOR IN BOTANY, THE UNIVERSITY OF CHICAGO

ILLUSTRATED

NEW YORK
D. APPLETON AND COMPANY
1903

CopPYRIGHT, 1903
By D. APPLETON AND COMPANY

Published July, 1903

PREFACE

In 1901 we published the first part of a work entitled
Morphology of Spermatophytes, containing an account of the
Gymnosperms. At that time it was our purpose to issue as
a second part an account of the Angiosperms, which would also
contain a complete index of the whole work. We have become
convinced, however, that such an association of these two great
groups would help to emphasize a relationship that does not
exist, and that Gymnosperms and <Angiosperms should be
treated as independent groups, coordinate with Pteridophytes.
Therefore, the present volume is issued, not as Part II of
Morphology of Spermatophytes, but as an independent volume
entitled Morphology of Angiosperms; and any subsequent
edition of the previous volume will be entitled Morphology of
(rymnosperms.

This volume, as the preceding, has grown out of a course
of lectures accompanied by laboratory work, given for several
successive years to classes of graduate students preparing for
research. It seeks to organize the vast amount of scattered
material so that it may be available in compact and related
form. While careful attention has been given to citations, so
that the student may know the groups that have been inves-
tigated, and be put in touch with the original papers, the work
is in no sense a compilation. The ground has been traversed
repeatedly, for several years, by various members of the botan-
ical staff and by numerous students, and their results have
served to check current statements, as well as to contribute no
small amount of new material.

vi MORPHOLOGY OF ANGIOSPERMS

Any one who has attempted to review the literature of the
morphology of Angiosperms will appreciate the great amount
of labor it involves, as well as the chaotic condition of termi-
nology and citations. There is nothing more batting than the
attempt to follow the guidance of the meager, indefinite, and
often incorrect citations of the standard texts. It is believed,
therefore, that the attempt to reduce the numerous contribu-
tions to a consistent terminology and to make the citations
fairly representative of the subject as well as definite and accu-
rate will be of some real service to students of morphology.
The volume, therefore, seeks to give to the advanced student a
continuous account of the structures involved, and to the research
student the details of groups and bibliography that he needs.

In every case where figures have been copied, acknowledg-
ment is made and a reference is given to the original paper
containing the illustration. It should be noted that much in-
formation included in the legends does not appear in the text,
so that in any thorough reading of the book the legends should
be included. The bibliography pertaining to each subject is
printed in chronological order at the end of each chapter con-
taining numerous citations. At the close of the volume all of
the cited bibliography is brought together, arranged alphabet-
ically by authors.

It would be too large a task to include a complete bibliog-
raphy of such a subject, but we have presented what may be
regarded as a full representative bibliography, containing, so
far as we know, all of the most important contributions. In
the very nature of things, some citations may have been
omitted that should have been included, but there has been
no intentional neglect.

No attempt is made to present the details of floral structure,
so fully deseribed by the earlier morphologists and taxonomists,
since they are easily accessible in numerous texts. Nor have
we ventured to enter the old and extensive field of anatomy,
although many of its details are pertinent to morphology. In

PREFACE vii

its later development, however, it has contributed so many
important data essential in any discussion of phylogeny that
we have asked Professor E. C. Jeffrey to present the general
outlines of the subject in the last two chapters of this volume,
a discussion which includes both Gymnosperms and Angio-
sperms. It is hoped that this presentation will help to stimu-
late the cultivation of an important field of research too much
neglected in this country.

It did not seem necessary to treat the two great groups of
Angiosperms separately. They are so similar in their essential
morphological features that their separate presentation would
have involved a needless amount of repetition. We have also
continued to regard the spore mother-cell as the end of the
sporophytic generation, and its division as the beginning of the
gametophyte. The reasons for this are more fully presented
in the present volume than in the preceding.

In the chapters upon classification we have presented the
scheme elaborated by Professor Engler, believing that it is
the best expression of current knowledge of relationship ap-
plied to the whole group, and that it is suggestive of the most
critical regions for research. This has not been pressed to the
dreary details of minor groups, for these are easily accessible.
It has rather been our intention to present the general ideas
involved in the alliances of first rank, so that principles rather
than details may be prominent. We have also thought that
the special student should be somewhat familiar with the his-
tory of the group, so far as known, its geographic distribution,
and the current notions as to its phylogeny. The last subject
may be regarded as more theoretical than profitable, but the
final aim of morphology is a definite phylogeny, and advance
toward it must be made by a succession of theoretical con-
clusions.

Joun M. Courter.

CuarLes J. CHAMBERLAIN.
THE UNIVERSITY OF CHICAGO,
January, 1903.

CONTENTS

CHAPTER PAGE
I.—INTRODUCTORY . ‘ : ‘ ‘ : : : : : : 1
Angiosperms and Gymnosperms contrasted, 1—Spermatophytes
not a natural group, 3—Monocotyledons and Dicotyledons con-
trasted, 4.

Il—Tue Frower . : ‘ ; : : : , ‘ ‘ ; 8
Definition of a flower, 9—Origin of floral leaves, 9—Tendencies
in the evolution of the flower, 10—Organogeny of the flower, 16
—Dioecism, 20—Morphology of floral members, 22—Stamen, 23
—Carpel, 24.

IL—Tse Microsporancium : : : : : F jy RT
Origin from periblem, 27—Cauline microsporangia, 283—Number
of microsporangia, 29—Time of formation, 30—Development,
32—Archesporium, 32—Parietal layers, 84—Tapetum, 36—
Mother-cells, 38—Dehiscence, 41—Line of demarcation between
sporophyte and gametophyte, 41.

IV.—TuHe MeGASPORANGIUM. ; ; ‘ : : ‘ , . 46
Origin from periblem, 46—Cauline ovules, 46—Foliar ovules, 50
—Morphological nature of ovule, 51—Time of development of
megasporangia, 52—Development of ovule, 53—Archesporiumn,
57—Parietal cells, 62—Mother-cell, 66.

V.—Tue FEMALE GAMETOPHYTE . é ; ‘ : ‘ : & atl
The tetrad, 71—Number of megaspores, 76—Reduction of chro-
mosomes, 80—The functioning megaspore, 84—Number of em-
bryo-sacs, 86—Germination of megaspore, 87—Variations in
history, 89—Egg-apparatus, 983—Synergids, 94-Fusion of polar
nuclei, 95—Antipodal cells, 96—Enlargement of enbryo-sac, 103
—The nutritive jacket, 103—Haustoria, 104—The mechanisin
for nutrition, 108.

VI—Tse Mate GaMETOPHYTE. . . . . . . . . 121

The tetrad, 121—Number of microspores, 125—The nuclear divi-
sions of the pollen mother-cell, 126—The microspores, 131—Ger-
mination of microspore, 132—Division of generative cell, 135—
The male nuclei, 136.

ix

x MORPHOLOGY OF ANGIOSPERMS

CHAPTER
VII.—FERTILIZATION . j :

Historical réswmé, 143—Development of pollen-tube, 146—Chala-
zogamy, 149—The pollen-tube within the embryo-sac, 151—Dis-
charge of pollen-tube, 152—Fusion of male and female nuclei,
153—Centrosomes, 1583—Double fertilization, 155—Male cell and
male nucleus, 160.

VIII.—Tue Enposrerm : 5 : : + . .
Contrast between Gymnosperms and Angiosperms, 165—The
fusion nucleus, 166—Endosperm without fusion, 166—Endo-
sperm and pollination, 167—Division of fusion nucleus, 169—
_Two methods of endosperm-formation, 171—Function of endo-
sperm, 179—Xenia, 179—Morphological character, 181—Nature
of triple fusion, 182.

IX.—Tue Empryo ; : : : ; : : 5 z .
Monocotyledons, 188—Alisma type, 188—Pistia type, 192—
Lilium type, 1983—Orchid type, 194—Dicotyledons, 196—Cap-
sella type, 199—Other types, 200—Degree of development, 205
— Pseudo-monocotyledons,” 206—Phylogeny of the cotyledon,
208—Parthenogenesis, 210—Polyembryony, 213.

X.—CLASSIFICATION OF MoNnocoTYLEDONS
Spiral series, 228—Cyclic series, 234.

XI.—CassiFicaTion of ARCHICHLAMYDEAE
XIL.—CLAssIFICATION OF SYMPETALAE

XIII.—Grocrapuic DistRIBUTION OF ANGIOSPERMS . ‘ :
Monocotyledons, 262—Archichlamydeae, 266—Sympetalae, 268.

XIV.—Fosstb ANGIOSPERMS s ‘ ‘
Monocotyledons, 2'772—Dicotyledons, 276.

XV.—PHYLOGENY OF ANGIOSPERMS , : : : *
Are Angiosperms monophyletic? 280—Relation to Gymno-
sperms, 283—Relation to Pteridophytes, 285—Theories of alter-
nation of generations, 288—Theory of the strobilus, 288—The
mutation theory, 292.

XVI—ComPaRATIVE ANATOMY OF THE GYMNOSPERMS AND THEIR ALLIES
Pteridophytes, 296—Cycadofilices, 300—Cycadales, 304—Ben-
nettitales, 306—Cordaitales, 307—Ginkgoales, 307—Coniferales,
308—Gnetales, 310.

XVIT—Comparative ANATOMY OF ANGIOSPERMS
Dicotyledons, 311—Monocotyledons, 314.

PAGE

143

165

187

wv
oO
oO

MORPHOLOGY OF ANGIOSPERMS

CHAPTER I

INTRODUCTORY

Tuere is a very large element of uncertainty in a presenta-
tion of the special morpholee ry of Angiosperms, chiefly because
of the vast amount of unstudied material, but also because of
the inequality in the accuracy and definiteness of the work
done. However, the general outlines seem to be fairly well
established, and their filling in must long oceupy morphologists.

Although two very distinct groups of Angiosperms are
recognized, the Monocotyledons and the Dicotyledons, their es-
sential morphology is so similar that separate treatment would
involve needless repetition. The chief differences between them
have to do with the structure of the vegetative body of the
sporophyte. A general treatment of these differences is not
necessary in a book dealing with special morphology, for it
belongs to elementary instruction; while a special treatment
would lead into the immense field of anatomy, which it is not
the purpose of this book to present. So far as anatomical
studies have a conspicuous bearing upon the phylogeny of the
great groups, they are presented by Professor E. C. Jeffrey
in the last two chapters. :

In contrasting Angiosperms with Gymnosperms, one is im-
pressed by the fact that a group of plants comprising more
than one hundred thousand known species can not be presented
with the same confidence and detail as can a group represented
by-a-scant four hundred species. And yet, what have been
agreed upon as the essential morphological features of these
groups appear to be more uniform in Angiosperms than in
Gymnosperms. In our treatment of the latter group, the great

1

2 MORPHOLOGY OF ANGIOSPERMS

divisions were presented separately because of the diversities ;
but the morphological diversities among Angiosperms seem to
be not so much those of groups as of habit and habitat. While
it is generally agreed that the seed-bearing habit was devel-
oped independently in more than one phylum, and that the
Gynmosperms and Angiosperms have probably no immediate
phylogenetic relation to one another, it is of interest to note
the essential contrasting features of the two great seed-bearing
groups.

The chief contrast in the sporophyte is that in Gymno-
sperms pollination results in bringing the pollen in contact
with the ovule, while in Angiosperms the result of pollination
places the pollen in contact with a receptive surface developed
by the carpel. This contrast involves great differences in mor-
phological structure, so great, in fact, that it is hard to imagine
one of these conditions as having been derived from the other.
The method of pollmation might also be mentioned as a con-
trasting feature, since the primitive anemophilous habit seems
to be universal among the Gymnosperms, while among Angio-
sperms it prevails only among those groups that may be re-
garded as primitive. There accompanies this contrast a similar
one im connection with the flower. Just how this structure
may be defined is considered in the next chapter, but the char-
acteristic flowers of Angiosperms have no representative among
Gynmosperms, however much the older morphology felt com-
pelled to homologize them. However, the method of pollination
and the flower are but corollaries to the fundamental contrast
involved in the contact of the pollen with the ovule in the one
case, and with the carpel in the other.

A second fundamental distinction in connection with the
sporophyte is to be found in the embryogeny of the two groups.
In the Gymnosperms, the free nuclear division within the fer-
tilized egg, and the use of the bulk of the ege as a food re-
serve in most forms are in sharp contrast with the absence of
free nuclear division in the Angiosperm egg, a character ap-
pearing, however, in Gnetum and Tumboa.

If the contrast between the sporophytes of Gymmnosperms
and Angiosperms be pressed into anatomical details, the differ-
ences are found to be quite as striking, though perhaps a little
more perplexing.

INTRODUCTORY 3

The contrast between the gametophytes of the two groups,
especially the female gametophytes, is even greater than that
shown by the sporophytes. The male gametophytes of Gymno-
sperms when contrasted with those of heterosporous Pterid-
ophytes present a much shorter history; and the gametophytie
structure produced by the Gymnosperm microspore involves
the formation of two or three times as many cells-as are formed
in the germination of the Angiosperm microspore. The female
gaimetophytes of the two groups, however, are in the main stri-
kingly different. As is well known, the female gametophytes
of Gymnosperms in general, with their well-organized tissue
and archegonia, are almost the exact counterparts of those of
Selaginella and [soetes; while the female gametophyte of An-
giosperms remains a morphological puzzle, made still more
perplexing by the discovery of the wide-spread phenomenon
styled ‘‘ double fertilization.” It is a very significant fact, how-
ever, that in spite of the difficulties of the female gametophyte
of Angiosperms in the way of interpretation and of origin, it
is one of the most remarkably consistent structures known to
morphology, the sequence of events in its history representing
an almost unvarying schedule, and supplying one of the strong-
est arguments in favor of the monophyletic origin of Angio-
sperms.

In view of these and other differences between Angiosperms
and Gymmosperms, the question is raised whether we have not
been too narrow in the conception of the seed-bearing habit in
compelling these two groups to remain as subdivisions of a
group Spermatophytes coordinate with Pteridophytes and
Bryophytes. In a certain sense, to select a single character,
such as seed-bearing, as a basis for the union of two groups
otherwise dissimilar is suggestive of artificial classification.
Furthermore, to separate the female gametophytes of Gymno-
sperms from those of the heterosporous Lycopodiales, and to
associate them with those of Angiosperms, is certainly to do
violence to a most important suggestion of natural relation-
ships. In our judgment, therefore, the designation Sperma-
tophytes should be used in a general way, as a term of con-
venience rather than of classification, only less extensive in its
application than “vascular plants”; and Gymnosperms and
Angiosperms should be recognized as two groups coordinate

4 MORPHOLOGY OF ANGIOSPERMS

with Pteridophytes and Bryophytes. In fact, Pteridophytes
and Gymnosperms together form a much more natural group
than do Gymnosperms and Angiosperms; and this fact should
be emphasized by treating Gymnosperms and Angiosperms as
eroups of the first rank.

Although it is a question whether Gymnosperms and An-
giosperms should be so closely associated:as to form the two
subdivisions of a great group, there can he no question that
Monoeotyledons and Dicotyledons are naturally and intimately
associated. This proposition is not affected by the question of
their common origin, but is based upon their essential mor-
phological features, whatever may have been their origin. The
characters that separate Monocotyledons and Dicotyledons are
cumulative rather than specific, and although the character of
the embryo is held to be the decisive one in every case, there is
danger of using it with unnatural rigidity. When a decision
between two groups is reduced to a single character, there is a
suspicion either that the groups can only be separated arti-
ficially or that too much stress is laid upon the character. Mon-
ocotyledons and Dicotyledons are best distinguished by cer-
tain tendencies that involve several characters, and if these
tendencies are supported by the character of the embrvo the
case is clear. A brief statement of the conspicuous differences
may be of service.

1. In the embryo of Monocotyledons the cotyledon is ter-
minal and the stem tip lateral in origin; while in Dicotyledons
the stem tip is terminal and the cotyledons lateral in origin.
This character seems to be fundamental, and at the present time
is the only one that may be regarded as decisive. That the
difference indicated will always be expressed in the above
terms is not likely, for the nature of the cotyledon is in ques-
tion, and the significance of this relation of parts has vet to be
determined,

2. The development of the vascular bundles in the stele is
very different in the two groups. This difference involves not
only the arrangement of the bundles, but also the presence or
absence of fascicular cambium, and is far-reaching in its re-
sults upon the habit of the body. In the case of perennial
stems it involves the general ability to inerease in diameter,
and this affeets the power of branching, and this in turn deter-

INTRODUCTORY 5

mines the question of an annual increase in the display of
foliage, which means the working power of the body. This
character can not be used as a specific test for the two groups;
nor must it be pressed in certain features alone or too rigidly.
When intelligently applied, it is probably only second in im-
portance to the character supplied by the embryo; but it must
be remembered that these prevailing tendencies of the two
groups are in some instances exchanged.

3. The characteristic foliage leaves of Monocotyledons have
a closed venation, while in Dicotyledons the venation is open.
This character involves many differences in detail. For ex-
ample, as a result the Monocotyledon leaf is entire, while the
Dicotyledon leaf, with veins ending freely in the margin, is
inclined to branch more or less, this tendency expressing itself
in the greatest variety of ways from simple teeth to the so-
called ‘* compound leaves.” * It is also true in general that in
Monocotyledons there is a sharp contrast in size between the
principal veins of the leaf and the reticulating veinlets; while
in Dicotyledons the gradation is so gradual that the reticulation
becomes very evident. It may be well to call attention to the
fact that while the so-called ‘ parallel”? venation may be of
service in distinguishing the majority of Monocotvledons in
temperate regions, as contrasted with the “‘ pinnate” or “ pal-
mate”? venation of Dicotyledons, it loses its significance when
‘the tropical Monocotyledons are included. The distinctive
character of closed or open venation can not be applied to all
Monocotyledons and Dicotyledons, and is certainly less gen-
eral in its application than the two characters already given.
As a character to be used in a cumulative way, however, it
deserves prominent mention.

4+. Among Monocotyledons and Dicotyledons with cyclic
flowers the establishment of three as the cycle number of the
former, and of five or four as the cycle number of the latter
is quite distinctive. In fact, the constancy with which these
numbers appear is more remarkable than the exceptions. Of
necessity, this character is of comparatively limited use, but
it is of service among the cyclic families, and also among those
families some of whose floral parts are in cycles. The persist-

* This term should be abandoned for leaves, as has the term ‘‘ compound
flower” for the characteristic head of Compositae.

6 MORPHOLOGY OF ANGIOSPERMS

ent tendency of the spiral groups of Monocotyledons and Dicot-
yledons to express the appropriate cyclic number, when the
conditions seem to favor indefinite numbers, is even more re-
markable than the constant reappearance of the cyclic number
in families in which it has become established. Just what has
determined these numbers for the two great groups is an inter-
esting but unanswered question. The problem is confused by
the fact that certain plants, undoubtedly Monocotyledons or
Dicotyledons by all the usual tests, have the cycle number of
the other group.

In addition to the distinguishing characters enumerated
above, others of much less general application have been sug-
gested, but it is not clear that any of them are really significant
group characters.

There are certain general differences in the leaves of the
two groups that deserve mention, since they come as near rep-
resenting group tendencies as any of the secondary characters
just enumerated. Among Dicotyledons the foliage leaf is gen-
erally more differentiated than among Monocotyledons, inclu-
ding a petiole and often stipules. In fact stipules would be
quite characteristic of Dicotyledons were they not lacking in
so many, for Monocotyledons possess no such structures.
Among the latter, however, there is the almost equally char-
acteristic leaf-sheath from which the blade directly arises.
This general distinction between the leaves of the two groups
must have some unappreciated significance, and suggests that
it may represent something as fundamental as do the differ-
ences in the embryo and the stele.

The so-called “‘ germination” of the seed is suggestive of
different tendencies in the two groups, but the data seem to
be too scanty and indefinite as vet for safe generalization. So
far as they do exist, they indicate a tendency in Monocotyledons
to free the stem and root tips by the elongation of a portion
of the cotyledon, the other portion remaining in contact with
the endosperm as a digesting and absorbing organ, very sug-
gestive of the “ foot” of Pteridophytes; while in Dicotyledons
the tendency is to liberate the growing points and cotyledons
by the elongation of the hypocotyl, and even hypogean cotyle-
dons are not related to endosperm as digestive and absorbing
organs.

-~T

INTRODUCTORY

It is claimed that the prophyllum * of Monocotyledons is
solitary and posterior, while in Dicotyledons there are two op-
posite and lateral prophylla. If such structures generally
occurred, or even if this distinction were generally true when
they do oceur, such a character would be significant, for the
prophyllum certainly has a definite connection with the position
ot the successive floral parts in relation to the main axis.

It has been urged also that the Monocotyledons are char-
acterized by a small embryo embedded in an abundant endo-
sperm, and that in Dicotyledons the tendency is to develop
larger embryos at the expense of the endosperm. This involves
so many and such important exceptions that it can hardly be
regarded as a distinction between these two great groups.

The roots of Monocotyledons are said to differ from those
of Dicotyledons in that the primary roots are short-lived and
there is no persistent root-system as in many Dicotyledons.
While this may be true of Monocotyledons in general, it is also
true of many Dicotyledons, and can not be used as a distinct-
ive character.

All the characters enumerated above, both those of primary
and those of secondary importance, are to be considered in any
general characterization of the two groups; but it must be re-
membered that most of them await confirmation as essential
group characters. It is of interest to note that they are all
characters of the vegetative sporophyte, and that the sporangia
and gametophytes of Monocotyledons and Dicotyledons have
thus far given no tangible evidence of group differences.

* Translated into German as Vordlatt, and into English as fore-leaf. The
first leaf on a branch, but used only in connection with the bractlets of a
flower cluster.

CHAPTER II

THE FLOWER

Tur morphology of the flower of Angiosperms has an enor-
mous literature, much of which is now more curious than valu-
able. It is not the purpose of this book to present the numerous
details and extensive terminology that were so conspicuous a
feature of the older morphology, dominated as it was by the
doctrine of metamorphosis. For these the student is referred
to Eichler’s Bliithendiagramme (187578), in which may be
found the most complete account of the flower of Angiosperms
from this standpoint. The English student will also find an
admirable short account of the same subject from the same
standpoint in Gray’s Structural Botany (1879). A presenta-
tion that combines much of the older method of treatment with
newer points of view appears in Goebel’s Outlines of Classi-
fication and Special Morphology of Plants (English transla-
tion, 1887). Among the later important literature the follow-
ing may be consulted: Goebel’s Vergleichende Entwicklungs-
geschichte der Pflanzenorgane in Schenck’s Handbuch der
Botanik (31: 99-432. figs. 126. 1884); Celakovsky’s Ueber
den phylogenetischen Entwicklungsgang der Blitte und uber
den Ursprung der Blumenkrone, I and IT (Sitzber. Konigl.
Bohm. Gesell. Wiss. 1896 and 1900); Familler’s Biogenetische
Untersuchungen iiber verkiimmerte oder umgebildete ‘Sexualor-
gane (Flora 82: 133-168. figs. 10. 1896); Engler and Prantl’s
Die Natiirlichen Pflanzenfamilien ; Goehel’s Organographie der
Pflanzen (vol. ii, 1901).% These works and others like them
must be consulted for the details of the structure of angio-

* Tt should be understood that in this mention of the literature of the
flower only certain important works are cited, and that only in the subse-
quent chapters is there any attempt at presenting fairly complete lists of the
important literature.

8

THE FLOWER 9

spermous flowers, for in this chapter only certain of the broader
morphological features will be discussed.

Any strict definition of a flower seems to be impossible.
That the morphological precursor of the angiospermous flower
was some such structure as the strobilus of Pteridophytes seems
reasonably clear. In fact, the strobilus is plainly continued
among the Angiosperms in spiral flowers and spirally arranged
members. The appearance of distinct floral leaves associated
with sporophylls, however, is characteristic of the higher An-
giosperms. If a flower is essentially a sporophyll or a set of
sporophylls, as the older definition insists, Pteridophytes must
be included among flowering plants. If, on the other hand, a
flower is characterized by floral leaves, many Angiosperms are
not flowering plants. In any event, the term flower is of indefi-
nite application, and is incapable of sharp definition. It is a
term of convenience among Angiosperms, where it also in-
cludes strobili. The attempt of the older morphology to estab-
lish a definite conception for a flower, and to force all of the
sporophyll-bearing structures of Seed-plants into this concep-
tion was exceedingly unfortunate.

The development of floral leaves among Angiosperms seems
to be connected with the evolution of entomophily, which has
resulted in immense diversity in the details of floral structure,
but such details are quite foreign to the purpose of this book.
The origin of floral leaves, however, is a question that must
be considered.

That all floral leaves are derived from sporophylls may be
said to be the current view, as stated by A. P. De Candolle in
1817, and by many subsequent writers, notably Celakovsky in
1896 and 1900. Goebel, however, in his recent Organogra-
phie der Pflanzen, claims that while in a large number of cases
floral leaves may be derived from sporophylls, as in Nymphaea,
ete., they are often derived from “ bracts.” For example, he
calls attention to certain anemones in which the involucre be-
comes the calyx and this in turn may become petaloid. In other
words, he claims a double origin for floral leaves, namely, spo-
rophylls and foliage leaves, and whichever their origin the
result is the same. It may be of interest to note that Goebel’s
definition of a flower, a definition originally proposed by
Schleiden, is “a shoot beset with sporophylls,” which of course

10 MORPHOLOGY OF ANGIOSPERMS

includes certain Pteridophytes among flowering plants. It is
certainly more in accord with present morphological concep-
tions not to limit too rigidly the possible origin of a structure,
and from this point of view it seems reasonable that floral leaves
in general may have been derived from contiguous structures
both above and below.

It is not always easy to delimit a flower exactly from the
vegetative shoot, for there are numerous illustrations of grada-
tions between foliage and floral leaves; but for all ordinary
purposes four different organs are readily recognized as enter-
ing into the structure of a highly developed flower. The dis-
carded doctrine of metamorphosis assumed that such a flower
is the type, from which all others are the modified descendants,
and this conception is perpetuated in terminology. The same
conception dominates also in nearly all presentations of floral
diversities, as it is well-nigh impossible to abandon at once all
the terms of an obsolete conception and remain intelligible.
It has been a very prevalent conception, therefore, that flowers
of simpler structure than the assumed type are reduced forms.
There are certain cases in which this seems clear, as in the
relation of Lemna to the Araceae; but the vast majority of
simpler flowers are better regarded as primitive than as re-
duced forms. At present this is at least a valuable working
hypothesis, for it coincides in general with the morphological
and historical evidence concerning relationships, as well as
with the doctrine of evolution.

Accepting the evidence that the simpler flowers are for the
most part the more primitive forms rather than reduced ones,
certain prominent tendencies in the evolution of the flower,
admirably presented by Engler, may be discussed. It must be
understood, however, that only general tendencies are traced,
for the actual lines of descent can not be determined by our
present knowledge.

The naked flower with one or more free sporophylls may
be regarded as the most primitive form. In fact, it is an
angiospermous flower without the characteristic floral leaves.
Such a flower may sometimes represent a case of reduction,
but its persistent association with plants recognized as primi-
tive from other testimony is very strong evidence that it is a
prunitive condition of the flower. From this stage a series

THE FLOWER 11

‘an be arranged illustrating the gradual development and dif-
ferentiation of the two floral envelopes. Foliar members,
whether derived from foliage leaves or sporophylls, become
more and more definitely associated with the sporophyls, until
they may be regarded as constituting an inconspicuous, bract-
like perianth. They gradually appear in two definite sets and
become more conspicuous, and sooner or later show the petaloid
texture and coloration. The final stage is a completely differ-
entiated calyx and corolla, with their characteristic differences.
This tendency to produce a completely differentiated calyx and
corolla has resulted in its attainment by most flowers, but there
are numerous cases in which even near relatives have not made
the same progress in this regard. For example, the phenom-
enon styled apetaly may be observed in flowers whose nearest
relatives have a distinct calyx and corolla. While some cases
of apetaly may be explained as the suppression of a set of floral
envelopes, there are certainly cases in which it means that the
two sets have never become differentiated. This indicates that
progress made in a single direction can not be used as a eri-
terion of relationship. In general, however, it must remain
true that a flower with completely differentiated calyx and
corolla, other things being equal, is of higher rank than a
flower which has not attained this differentiation.

Among the most primitive flowers the floral axis tends to
elongate, and the members appear in indefinite numbers along
a low spiral. In more highly developed flowers the growth of
the axis in length is checked at a very early period, so that the
spiral along which the members successively appear becomes
lower and lower, until it has only a theoretical existence, pass-
ing into successive cycles, which eventually become limited in
number. With the appearance of definite cycles the number of
members appearing in each one becomes limited, the limit in
Monocotyledons being prevailingly three, and in Dicotyledons
five or four. It is to be noted that the cyclic arrangement is
not attained simultaneously by all the sets of a single flower.
For example, in many species of Ranunculus the sepals and
petals are cyclic, or approximately so, while the stamens and
carpels are distinctly spiral. This tendency is so well-marked
and so uniformly displayed that Engler has used it as a basis
for dividing Monocotyledons into two great series, the “ spiral

12 MORPHOLOGY OF ANGIOSPERMS

series ” comprising all those families that show the spiral tend-
ency in any of the floral sets, and the ** cyclic series”? compris-
ing all those whose flowers are completely cyclic, the former
series including all the more primitive families. There is no
reason why this same distinction can not be applied also im a
general way to the Archichlamy deae. This gradual transition
of flowers from the spiral to the cyclic condition is one of the
best-marked tendencies in their evolution, and has the advan-
tage of being represented by innumerable intermediate stages.
All of those families which are recognized as being of the high-
est rank have completely cyclic flowers, with members appearing
in definite and low numbers, notably illustrated by the whole
group Sympetalae.

There is a marked tendency in flowers for the members
of a single set to lose their identity and to develop en masse,
a phenomenon called “ coalescence” by the older morphologists,
under the impression that separate members had united. This
congenital union is to be distinguished from such a mechanical
union as is shown by the anthers of Compositae. In the organ-
ogeny of such a flower it is to be observed that in the meriste-
matic zone from which a certain set is to develop, the different
members first appear as separate primordia, but sooner or later
the whole zone shares in the growth and, the axial growing
point being checked, an annular structure arises that gradually
assumes the size and form of the mature organ (Fig. 1). It
has been claimed that this is a toral uprising and that, for
example, the tubular portion of a sympetalous corolla is mor-
phologically torus, but there secms no more reason for this
supposition than to regard an individual petal as a toral up-
rising. It is merely the difference between development from
the meristematic zone at certain points and at all points. As
is well known, this development of the whole zone may begin
almost at once, or may be deferred until the set is nearly mature,
resulting in every stage of separation in the members, from a
completely tubular structure to one that is tubular only at base.
Or the zone may develop for a time in two sections and later
en masse, resulting in the so-called bilabiate structure. Further
inequalities in the time and rate of dey elopment result in

various irregularities. In any event, this tendeney to zonal
development rather than the maintenance of separate points of

THE FLOWER 13

development is persistent among flowers, the first set showing
it being the carpels, resulting in syncarpy. The zonal develop-
ment of the corolla, however, or sympetaly, accords with so
many other characters indicating natural relationships that it
has been used to designate and even to define the great group
Sympetalae. This is probably pressing a single character too
far, tor there is evidence that the result has been to do violence
to certain natural relationships, and to make certain unnatural
groupings. This tendency to zonal development is found in
every floral set, and those flowers that show it are certainly
to be regarded as of higher rank than those that do not.

Among the more primitive flowers each cycle arises sep-
arately from the growing point, its members remaining separate
or the whole meristematic zone entering more or less completely
into the outgrowth. The insertion of each cycle is definitely
below that of the next inner cycle, resulting in an hypogynous
flower (Fig. 1, 4). That hypogyny is a primitive condition of
the flower is a statement that does not seem to need discussion.
The tendency to zonal development, however, is carried farther
when a whole region arising en masse produces two or more
cycles of floral members. In the simplest cases two cycles are
thus produced, as is illustrated by the strong tendency of the
petaliferous and staminiferous cycles to have a common origin
in sympetalous Howers, resulting in the appearance of “ stamens
inserted on the tube of the corolla.” The same tendency is
shown among orchids, in which the whole region for the devel-
opment of stamens and carpels arises in a single body, forming
the characteristic gynostemium or “ column.” While these may
be regarded as special tendencies of certain groups, rather than
of flowers in general, there are other instances that seem to
belong to the general evolution of the flower. In certain cases
the region of the growing point belonging to the carpels ceases
to develop, while the rest of the growing point continues to
develop en masse, forming a cup or urn-like outgrowth, from
the rim of which the three outer sets develop separately, form-
ing the periqgynous flower (Fig. 1, B). In this case the carpels
arise from what seems to be a depression in the center of the
torus, but which, of course, is the region of checked growth.
Perigyny is chiefly displayed among families of the Archi-
chlamydeae.

14 MORPHOLOGY OF ANGIOSPERMS

Far more general is the tendency to epigyny, in which the
checking of apical g erowth and the continued growth of the rest
of the growing point results im an ovule-bearing cavity grad-

Fie. 1.—“ Diagram to illustrate the morphology of typical flowers. A, hypogynous;
B, perigynous; C, epigynous; ), epigynous with prolonged ‘calyx tube.’ Recep-
tacle is dotted; carpels are cross-lined ; ‘ perianth tube,’ or ‘calyx tube, vertically
lined; sepals, petals, and stamens are unshaded, but may be distinguished by their
relative positions.” —After Ganona.*

ually roofed over by the earpels. From the top of the ovary
thus developed the four sets of floral members develop as usual,
those of each set remaining independent, or a eycle deve ‘loping

* Ganona, W. FF. The Teaching Botanist. New York. 1899.

THE FLOWER 15.

en masse, or two cycles (especially petaliferous and staminifer-
ous) having a common origin (Fig. 1,C, D). Goebel holds (Or-
ganographie) that at least in some epigynous flowers (as Pirus
Malus) the carpels do not merely roof the ovular cavity but also
line it, basing the claim upon a study of the meristematic tissue ;
in which case the wall of the so-called “ ovary” is toral without
and carpellate within. It is to be expected that numerous in-
termediate stages between complete hypogyny and extreme
epigyny will be displayed, as may be inferred even from the
doubtful phrases employed by taxonomists to describe them.
It also seems to be a safe conclusion, since epigyny is con-
stantly associated with the most specialized groups of each great
division, as Orchidaceae among Monocotyledons, Umbelliferae
among Archichlamydeae, and Clompositae among Sympetalae,
that it is a mark of higher rank than hypogyny in any evolu-
tionary series.

The tendency for the members of a floral set to develop
unequally, resulting in zygomorphy or various forms of “ irreg-
ularity,” is not general, and can not be applied so broadly as
can the tendency to the cyclic arrangement or to epigyny. In
certain groups, however, it is very pronounced as a special
character, as Orchidaceae among Monocotyledons, Lequmi-
nosae among Archichlamydeae, and Personales among Sympet-
alae. The occurrence of zygomorphy in relatively primitive
as well as in highly specialized groups indicates that it is to be
regarded as a special rather than a general tendency; and yet,
other things being equal, the zygomorphic flower is to be re-
garded as of higher rank in any given evolutionary series than
the actinomorphie flower. Diversities resulting from inequali-
ties of growth are often described in terms of symmetry, a
term that unfortunately has two applications in connection
with the flower, for its well-known biological use by Sachs
found it already used to designate a flower “in which the mem-
hers of all the cycles are of the same number.” In its biological
sense a symmetrical flower is one “that can be divided into
two similar halves, or the parts of which are radially disposed
around a central point.” The terms “ monosymmetrical” and
“ nolysymmetrical” are logical, but not better than the older
terms of Eichler, “ zygomorphic ” and “ actinomorphiec.” How-
ever, the phenomena of floral symmetry are not well expressed

16 MORPHOLOGY OF ANGIOSPERMS

in two categories, and three have been proposed, as follows: (1)
actinomorphic, in which the planes of symmetry are as numer-
ous as the members of a cycle; (2) tsobilateral, in which there
are two planes of symmetry, but the halves produced by one
plane are unlike those produced by the other (Dicentra, Cru-
ciferae, ete.) ; and (3) zygomorphic, in which there is only one
plane of symmetry (Fig. 2). These categories are expressions

of certain laws of growth, and that they are somewhat funda-

Fie. 2.— 4, radial symmetry (Lilium tigrinum),; B, isobilateral symmetry (Capsella
Bursa-pastoris) ; C, zygomorphie symmetry (Scrophularia nodosa).

mental may be inferred from the fact that they are persistent
through great groups of plants.

While these and other evolutionary tendencies are to be
observed among flowers, it is evident that they are not neces-
sarily expressed simultaneously. For example, the spiral and
cyclic arrangements are associated in Ranunculus, zygomorphy
is associated with polypetaly and hypogyny among the papil-
lonaceous Leguminosae, epigvny is associated with polypetaly
among the Umbelliferae, and sympetaly and zygomorphy are
associated with hypogyny among the Labiatae. It is among
the Compositae that practically every evolutionary tendeney
mentioned finds its highest expression. Tt is only by striking
an average that such characters may be used in roughly placing
a family in its evolutionary position, commonly called. its
“yelative rank.”

The classie memoir on the organogeny of the flower is
Payer’s Traité Vorganogénie de la fleur (1857), but the sub-
ject has not been developed since as it deserves. Tn the case
of spiral flowers, in which the torus elongates more or less, the

Fic. 3.—Cnicus arvensis. Floral development: A, receptacle almost evenly convex; B,
appearance of papilla to become flowers; C, a single papilla more advanced, show-
ing beginning of corolla; D, corolla more prominent; Z, stamens distinguishable ;
F, carpels and pappus (calyx) evident; G, carpels beginning to form cavity of
ovary ; /, ovule readily distinguishable; /, ovule showing megaspore mother-cell
and single thick integument: 4, bract of involucre; c, corolla; s, stamen; 0, carpel;
Pp, pappus (ealyx). A-/ x 50; J x 100,

18 MORPHOLOGY OF ANGIOSPERMS

members appear in acropetal succession along a continuous low
spiral, and just when one set of members stops and the next
begins is indefinite within certain usual limits. There seems
no doubt in this case that the primordia are indifferent up to
a certain stage of development, and that the particular organ
produced depends upon something outside of the essential con-
stitution of the primordium itself. In the case of cyclic flowers,
in which toral growth in length has been checked and there has
been growth in diameter, the acropetal succession of members
is often very much interfered with. The “ disturbances” that
arise in the torus by substituting growth in diameter for growth
in length account not only for the breaking up of the acropetal
succession, but also for the inequality of members. of the same
cycle, or of different regions of the cycle. It is evident that in
the case of cyclic flowers organogeny must deal not only with
the succession of cycles, but also with the succession of mem-
bers in each cycle. Definite data in reference to these points
are not so available as they should be, but a few illustrations
may be cited.

For the majority of cyclic flowers it seems to be assumed
that the cycles appear in acropetal succession—namely, sepals,
petals, stamens, carpels—and that the members of each cycle are
practically synchronous in origin, but it is probable that this
assumption is gratuitous. While theoretically it may be as-
sumed that the cyeles should arise in acropetal succession, the
fact that they do not in many observed cases indicates that
they may not in many more cases; and the synchronous ap-
pearance of the members of a single cycle is unsound as a
theoretical assumption. Hofmeister * records that in Rosa,
Potentilla, and Rubus the primordia of the carpels appear be-
fore those of the stamens have reached the full number, and
that in Hypericum calycinum the primordia of the sepals ap-
pear after those of the stamens. It is also generally known
that among the Compositae (Fig. 3), Dipsaceae, Valerianaceae,
and Rubiaceae, in which the sepals are much reduced or modi-
fied, their primordia do not appear until after those of the
stamens and carpels; and that among the Cruciferae (in Cap-
sella, at least) (Fig. 4) the petals are the last members to

* Hormerister, W. Allgemeine Morphologie der Gewiichse. Leipzig. 1868.
ay §
p. 462.

THE FLOWER 19

appear. Webb* has recently observed in Astilbe that the
order of succession of floral cycles is sepals, inner stamens, car-
pels, outer stamens, and petals. In this case there is an acro-

Fic. 4.—Capsella Bursa-pastoris. Floral development: A, floral axis before appearance
of floral organs; &, appearance of sepals; (, appearance of stamens ; carpels barely
distinguishable ; D, appearance of petals: s, sepals; m, stamens ; ¢, carpels ; p, petals
x 130.

petal succession of certain cycles, followed by a basipetal succes-
sion of the remaining ones. The remarkable case of the flower
of the Primulaceae, noted by Pfeffer,+ is also familiar, in
* Wess, J. E. A Morphological Study of the Flower and Embryo of Spi-
raea. Bot. Gazette 33: 451-460. figs. 27. 1902. For correction of names, see
Renper in Bot. Gazette 34: 246. 1902.
. + Prerrer, W. Zur Bliithenentwicklung der Primulaceen und Ampelideen.
Jahrb, Wiss. Bot. 8: 194-215. 1872.

20 MORPHOLOGY OF ANGIOSPERMS

which the primordia of the petals appear after those of the
stamens, and each apparently from the dorsal surface of a young
stamen. The conclusion that the so-called petals of this family
are not morphologically petals, but stamineal outgrowths, is
unnecessary, since the phenomenon can be more logically in-
terpreted as a case in which the primordia of stamen and petal
have a common origin, entirely analogous to the sympetalous
corolla with stamens “ inserted on its tube,” but in which the
separate primordia of the petals have been delayed in their
appearance. Such examples as those enumerated above simply
serve to emphasize the desirability of a more serious and sys-
tematic investigation of the whole subject.

In the case of members of a single evele, it is a question
whether their primordia ever appear simultaneously, although
they may appear in rapid succession. In zygomorphic flowers,
however, the snecession is probably always evident. For ex-
ample, Goebel * cites the case of the papilionaceous Legumino-
sae, in which the anterior median sepal first appears, then those
to the right and left of it simultaneously, and finally the two
obliquely posterior ones; but before these last are evident the
two obliquely anterior petals appear, and after them the other
three in the same order as the corresponding sepals. This
succession proceeds right and left from the anterior member
to the posterior. In other known cases, however, as in Reseda,
according to Payer, the succession is right and left from the
posterior member to the anterior.

It must also be noted that a meristematic zone giving rise
to a set of members may add to the set later or even duplicate
it, giving rise to the well-known interposition of new members
or new sets. For example, it is stated that among the Gera-
niaceae, Rutaceae, and Zygophyllaceae a new cycle of five sta-
mens is interposed among the five already formed; and that
in Aceraceae and Sapindaceae two to four stamens are inter-
ealated in the complete eyele of five previously formed. This
later interposition of new sets or new members has been ve-
corded chiefly for stamens, and is a prolifie source of inter-
ference with the “ symmetry ” of numbers.

All seed-bearing plants are necessarily dioecious since they
* Gorpen, C. Outlines of Classification and Special Morphology. Enelish
translation, 1887, p. 424.

THE FLOWER 21

are heterosporous. So far as there is any advantage in this
habit, however, it is practically lost if stamens and carpels are
present in the same flower or upon the same plant. Morpho-
logically the gametophytes are unisexual, but in fact they are
dependent upon the same individual. Any physiological advan-
tage, therefore, that comes from the crossing of individuals
must be secured by pollination or by the separation of stamens
and carpels upon different individuals. It is unfortunate that
the term “ dioecious” has two distinct morphological applica-
tions, referring to the sexual differentiation of individuals
among the lower plants, and to the sporangial differentiation
of individuals among seed-bearing plants; but from the phys-
iological standpoint the distinction probably does not exist. As
a consequence, the dioecious habit in effect is secured in certain
seed-plants by the development of monosporangiate individuals,
and it is perhaps significant that this habit not only prevails
among the more primitive seed-bearing plants, but is associated
in the main with wind-pollination. Among the higher Angio-
sperms the effect of the dioecious habit is secured for bisporan-
giate plants by means of insect-pollination. It follows from
this point of view that neither the monosporangiate nor the
bisporangiate habit can be regarded as in itself the more primi-
tive. The former habit prevails among the more primitive
families because they are necessarily anemophilous; while the
latter prevails among the higher families because insect polli-
nation does not necessitate the monosporangiate habit. It
should be noted that Goebel (Organographie) regards the
bisporangiate condition as primitive, the monosporangiate
being derived from it by reduction. This can be demonstrated
in certain cases, but the monosporangiate condition is probably
the primitive one in many of the more primitive angiospermous
families. In any event, the monosporangiate and bisporan-
giate habits are not always settled ones. For example, in the
monosporangiate Amarantus retroflerus there are occasional
bisporangiate flowers; while in monosporangiate and dioecious
willows both catkins may appear on the same individuals, and
the catkins themselves may be mixed (staminate, pistillate, and
bisporangiate). It follows also that there may be monosporan-
giate members in all great groups (as Ranunculaceae), or even
in bisporangiate genera (as Rumex and Lychnis), for this habit

5

Z MORPHOLOGY OF ANGIOSPERMS

L

is probably not a hindrance to any form of py lination, and cer-
tainly prevents self-pollination. Cross-pollination by wind or by
insects, therefore, appears as an offset to the loss of any advantage
originally gained by the dioecious habit; and the appearance of
monosporangiate individuals in any Angiosperm group does not
imply a tendency toward a more primitive or more advanced
condition. For example, the monosporangiate habit of poplars is
no more indicative of a primitive condition than is the monospo-
rangiate habit of certain Compositae of an advanced condition.

The older morphologists considered the floral members as
morphologically leaves, and presented proofs which to them
seemed decisive, such as the leaf-like position and intergrading
of members, and various malformations, among which are the
so-called “ reversions.” This conclusion was controlled by the
prevailing doctrine of metamorphosis, and under its guidance
nothing seemed clearer than that stamens and carpels are trans-
formed leaves. While sepals and petals may be regarded as
often leaves more or less modified to serve as floral envelopes,
and are not so different from leaves in structure and function
as to deserve a separate morphological category, the same claim
can not be made for stamens and carpels. They are very an-
cient structures, of uncertain origin, for it is quite as likely
that leaves are transformed sporophylls as that sporophylls are
transformed leaves. It is a rigid morphology, however, domi-
nated by the doctrine of “ types,” that denies to an organ so
thoroughly established as the stamen of Angiosperms a mor-
phological individuality. One might almost as well deny to
the leaf itself a morphological individuality because it did not
always exist as a distinct organ. Just how long an organ must
maintain its independence before it can be recognized as a
morphological unit is not easy to sav, but stamens and earpels
seem to have earned the right. To eall a stamen a moditied
leaf is no more sound morphology than to call a sporangium
derived from a single superficial cell a modified trichome. The

¢

cases of “reversion ’”’ cited are easily regarded as cases of re-
placement. Lateral members frequently replace one another,
but this does not mean that one is a transformation of the other.

For example, in 1889 Barber * observed a Nymphaea in which

* BarBer, C. A. Ona Change of Flowers to Tubers in Nymphaea Lotus,
var. monstrosa, Annals of Botany 4: 105-116, pl. 5. 1889,

THE FLOWER 23

foliage leaves had replaced all the floral members within the
calyx and the end of the axis had become much swollen. It is
probable that the latter fact was responsible for the former, and
that a growing axis put forth leaves, as it usually does; but the
inference that these leaves represent the replaced floral mem-
bers in any morphological sense has no logical connection with
the facts observed. Such cases as that of the ordinary flowers
of Nymphaea, in which stamens seem to be gradually differ-
entiated from petals, present no difficulty when one notes the
remarkable indifference of sporangia to the nature of the mem-
ber upon which they appear. Because microsporangia appear
occasionally upon an axial structure it might as well be argued
that stamens are transformed stems. The stamens and carpels
are just as definite morphological structures as are foliage
leaves, with just as distinct functions, and should be so re-
garded, whatever may have been their historical origin. Stamen
and leaf probably merge into one another in history, and so
do stem and leaf, but all have become established as distinct
organs.

Further details as to the varying form and structure of
sepals and petals are of no special morphological significance,
and are of interest chiefly to the taxonomist and the ecologist.
The stamens and carpels, however, are so intimately associated
with essential morphological structures that some further de-
tails in reference to them are necessary.

The stamen set has been called collectively the “ androe-
cium,” a name so objectionable to the morphologist on account
of its sexual significance that it should be abandoned. The
stamen is an organ devoted to the production of microsporangia,
and its endless diversity of form and position is related more
or less directly to the needs of pollination. The term “ anther ”
is one of convenience, but represents a morphological complex
made up of sporangia and more or less sporophyll tissue. The
cooperation of sporophyll and sporangia in the dehiscence of
the latter will be included in the discussion of the microsporan-
gium, as well as those various differences among anthers that
have to do with the number and behavior of their sporangia.
It is important to note that stamens have the power of branch-
ing, and can thus multiply sporangia. Well-known cases are
Callothamnus, in which the branching is lke that of a pinnate

3

24 MORPHOLOGY OF ANGIOSPERMS

leaf: Ricinus, in which repeated forking results in a stamen
bearing very numerous sporangia; and Hypericum, in which
the primordium branches, that 1s, produces secondary primor-
dia, the common base of the tufted cluster not being recognized
in the mature condition. The case of zonal development, that
is, an uprising from the whole staminiferous zone, and also the
ease of stamen and petal or stamen and carpel regions rising
en masse, have already been noted in connection with the gen-
eral tendencies of the flower. The tendency of stamens and
of carpels to become more or less coalescent through pressure is
also well marked, as in the anthers of Compositae and Lobe-
liaceae, and in some cases that have been called synearpy. It
remains to note the fact that stamens occur in all stages of
abortion, especially to be observed among the Personales, from
the absence of sporangia to that amount of abortion that is
only short of suppression. Stamens that have lost their normal
function are generally called “ staminodia,” but they may as-
sume various forms and serve a variety of purposes. In certain
cases, as notably among the Labiatae, the claim that one or
more stamens have been suppressed is justified by their pres-
ence in near relatives, combined with the occurrence of unoc-
eupied points where stamens ordinarily appear.

The carpel set has been called collectively the ‘ gynoecium,”
a term that also should be dropped from morphological ter-
minology on account of its implication of sexuality. The carpel
is the organ most intimately related to the megasporangia, in-
vesting them more or less completely, but not always producing
them, and giving name to the Angiosperms. Its history is un-
known, for although it is easy to imagine it derived from such
open ecarpels as are found among Gymnosperms, no clear inter-
mediate stages have been found. At all events, it is a thor-
oughly established and characteristic organ. The term “ ovary ”
for the sporangium-bearing cavity is particularly unfortunate
on account of its very different application among animals.
To avoid this confusion Barnes * has proposed the term “ ovu-

‘

lary,” but even this contains in its stem the sexual implica-
tion. The style is definitely related, in its varying form and
length, to the problem of pollination, and upon it the stig-

* Barnes, C. R. Plant Life. 1898. p. 240.

THE FLOWER 25

matic surface is developed in various ways. This surface is
increased in area by the enlargement of the apex of the style,
by its branching, or by being developed laterally upon the style.

One of the essential features of the structure of the carpel
is the provision for the progress of the pollen-tube from the
receptive surface to the sporangium or even to its micropyle.
A specialized and continuous nutritive tissue connects these
two extremes, often confused in the sporangial chamber with
the ‘‘ placenta,” in the style called “conducting tissue,” and
upon its surface the “ stigma,’ but forming one continuous
tissue system, well named the conducting tissue. It is unfor-
tunate that the terminology of taxonomy has somewhat di-
verted attention from the continuity of this tissue, for in it
the ‘‘ stigma” is an organ distinct from the style, rather than
a display upon the surface, often modified to receive it, of a
special tissue of the style. While the placenta is the point or
line of sporangium origin, and may be said to consist of spo-
ranglogenic tissue, it is probably true that much of the out-
growth that stands for the placenta to many is conducting
tissue. In the case of hollow styles, as in Lilium, Butomus,
Agave, Erythronium, Viola, Campanula, Sarcodes, etc., the
conducting tissue lines the canal as a glandular layer, or in some
cases, as in Anagallis, fills up a hollow style; but in most cases
the style is solid, with the conducting tissue as an axial strand.
In case a single style is connected with two or more sporangial
chambers, the strand of conducting tissue branches into each
chamber. This suggests the possibility that the stylar canal,
with its lining of conducting tissue, may represent a primitive
angiospermous condition, and that the larger development of
this tissue has resulted in the prevailing solid style, a view that
is also suggested by the development of the style. Of course
the reverse may be true, and the stylar canal a result of the
breaking down or rupture of the axial strand of conducting
tissue.

The strong tendency to a congenital development of carpels
has been previously noted, and this justifies the use of the term
“ nistil ” as one of convenience, although it does not stand for a
morphological unit. It is applied to any organization of car-
pels that appears as a single organ with one ovary, whether one
or more carpels are involved. It is to be noted that the term

26 MORPHOLOGY OF ANGIOSPERMS

“ovary ” also, as usually applied, has no definite morphological
significance, referring to a morphologically single sporangial
chamber or to a combination of several such units, and these
chambers may be of axial as well as of carpellary origin. The
various ways in which the congenital carpels are related to one
another in a compound pistil are of great service in taxonomy,
as the particular structure of such a pistil is usually charac-
teristic of great families, or even of groups of higher rank.
These details of structure are too fully presented in various
texts, however, to justify their repetition here. The relation
of sporangia to carpels is an important subject to the morpholo-
gist, and will be considered in connection with the development
of the sporangia.

CHAPTER III

THE MICROSPORANGIUM

THE microsporangia of Angiosperms are embedded struc-
tures, and are derived from the outermost layer of the peri-

blem. Thus far, the only recorded
exceptions to this origin are Naias
flexilis, and probably Zannichellia 1®
and Lilaea subulata,'’ whose micro-
sporangia are claimed by Campbell
to be derived from the plerome (Fig.
5). The periblem origin of the spo-
rangia seems to account for the fact
that the archesporium is superficial
in Pteridophytes and hypodermal in
Spermatophytes. It also accounts for
the indifference of the sporangia to
the morphological nature of the or-
gan upon which they appear. In
general, they occur upon a lateral
member that holds the same relation
to the axis as do the leaves, and in
this sense it may be called a leaf-like
member. Such sporangia, therefore,
may be called foliar, and the struc-
ture that bears them a sporophyll.
In certain cases, however, the sporan-
gia are derived from the periblem
of the axis, and such may be called
cauline. In each case the resulting
organ is a stamen, whether in the po-

Fie. 5.—Naias flewilis. A, young
stamen showing “integument ”
and plerome origin of arche-
sporium ; sporogenous cells rep-
resented with nuclei; x 200.
B, later stage; x 70.—After
CAMPBELL.!8

sition of a leaf or of an axis. The freedom with which micro-
sporangia are sometimes produced may be illustrated by the

27

MORPHOLOGY OF ANGIOSPERMS

(oe)

2

: ; Se sewer ; EVE arse
willows, notably Salix petiolaris, in which Chamberlain 1° found
microsporangia in the “ placenta ” of the ovary, the carpel some-
times being wide open and bearing both microsporangia and

CB C

Fic. 6.—Salix petiolaris. A, microsporangia in wall of ovary; both anatropous and
orthotropous ovules. B, microsporangia with long stalks within the ovary; pollen
normally developed ; ovule orthotropous. @, branching stamen, each anther with
four microsporangia; anther on right terminated by a stigma; x 50—After CHau-
BERLAIN,!6

megasporangia, and in some cases stigmas developing on sta-
mens (Fig. 6).

The cauline origin of microsporangia seems to have been
recorded first in 1868 in the case of Casuarina, by Kauft-
mann; ° and then in 1869 for the species of Naias, by Magnus,
confirmed in 1897 by Campbell.!° In 1873 Warming’ made
a similar record for Cyclanthera, and was confirmed by Eng-
ler® in 1876. Rohrbach * discovered cauline microsporangia
in Typha; Goebel? (p. 353) states that they oceur in the
“unbranched stamens’; and their oceurrence in T. latifolia
was confirmed by Schaffner ?? in 1897. In 1897 Campbell !®
added to the list Zannichellia, and in 1898 Lilaea.8 Tn 1900
Lotsy *° suggested that the curious stamen of Rhopalocnemis
phalloides (Balanophoraceae) is an axial strueture.

THE MICROSPORANGIUM 29

It is reasonably assured, therefore, that cauline micro-
sporangia occur in at least seven genera, both Monocotyledons
and Dicotyledons being represented. Upon the whole, they
seem more characteristic of the primitive members of these
two groups than of the more highly specialized members, but
this impression may disappear with further investigation. If
the cauline origin of megasporangia be considered, the primi-
tive character of this feature becomes increasingly uncertain,
for cauline megasporangia are common even in the highest
groups. It seems probable, therefore, that the cauline or foliar
origin of sporangia among Angiosperms is not to be taken as
an argument for or against the primitive character of the group
in which they occur. The particular organ developing micro-
sporangia was probably determined not by its morphological
nature, but by what may be called its physiological relations
(Fig. 6). Even among Pteridophytes, the sporangia of Lycopo-
dium are foliar, and those of the nearly allied Selaginella cau-
line; and among Gymnosperms sporangia have both origins.
It is evident, therefore, that the distinguishing morphological

Fie. 7.—Lilium philadelphicwm. Transverse section of almost mature anther; nearly
all the walls separating the microsporangia have broken down; highly developed
stomium (s) and endothecium (with its nib-like thickenings) very prominent; x 25.
—From a drawing by W. J. G. Lanp.

structure is the sporangium rather than any member of the
plant body from which it may arise.

In most ‘cases the stamen produces four microsporangia
(Fig. 7), and the exceptions noted thus far are by no means

30 MORPHOLOGY OF ANGIOSPERMS

numerous. Caldwell 2* has called attention to the occurrence
of what might be regarded a single microsporangium in Lemna ;
it is well known that the stamens of Asclepiadaceae produce
only two microsporangia; and in Hamamelis (Shoemaker 2)
there is a single sporangium to each “ pollen-sac.” Eight mi-
crosporangia had long been observed among the Mimoseae when
Engler ® reported a still larger number. Among the Orehida-
ceae Guignard?° reports eight microsporangia in the stamen
of Calanthe veratrifolia; and among the Onagraceae, as
in Gaura, more than four microsporangia are suggested by
the pollen-sacs (see Goebel,!! p. 369, footnote 2). Among
Loranthaceae Van Tieghem?* says that the number of pollen-
sacs is exceedingly variable, ranging from one to an indefinite
number; and the same is true of the Balanophoraceae, as re-
ported by several investigators. Attention should be called to
the fact, however, that the number of sporogenous masses finally
developed may not necessarily determine the number of spo-
rangia, for plates of sterile tissue, derived from sporogenous
tissue, have been observed to divide a single mass of sporoge-
nous tissue into two or more. This has been made out clearly
by Caldwell *? in the case of Lemna (Fig. 14); and in those
cases in which more than four microsporangia are reported a
detailed study of their origin is desirable. In the case of
branching stamens, referred to on p. 28, the microsporangia
may become very numerous.

The time for the formation of microsporangia in relation
to what is usually called “ the growing season” has not re-
ceived the attention it deserves. In 1896 Arma Smith? re-
ported that she had discovered the pollen mother-cells of Tril-
lium dividing in the spring beneath frozen soil. In 1897
Chamberlain 7° called attention to the fact that the microsporan-
gia of Salix glaucophylla are in the mother-cell stage in Oc-
tober, and that they pass the winter in this condition. In 1898
the same investigator 7° reported that this is true of other
species of Salix; that in Corylus americana (Fig. 8, B) and
Alnus glutinosa the midwinter catkins eontain pollen ready for
shedding with the generative cell formed: that in Populus
monilifera (Fig. 8, A) the primary sporogenous cells are
found in July and the mother-cell stage in October, the latter
condition persisting through the winter; and that in Hepatica

THE MICROSPORANGIUM bl

the mother-cell stage was found in September, and fully formed
pollen in the spring while the ground was still frozen. Dug-
gar ** has also observed that the microsporangia of Symplo-
carpus pass the winter in the mother-cell stage. The pollen
mother-cells of Podophyllum peltatum are forming the tetrads
when the young plant has reached the surface of the ground,
so that in all probability the winter is passed in the mother-cell
stage. Although Conrad *° found stamens well formed in the
winter buds of Quercus velutina,
the tissue of the anther was still
homogeneous. These records mere-
ly serve as an indication of what
may be expected when the subject
is really investigated. It is evident
that the time elapsing between the
differentiation of the arechesporium
and pollination is often much longer

than has been ordinarily supposed.
It would seem probable that in gen-
eral those plants whose flowers open
early in the season, as most trees
and the vernal herbs, develop their

microsporangia before the end of ESOT E EL bueg
the “ growing season,” and that the =) egos Gad sae
mother-cell stage is the usual win-
ter condition. In the ease of such B

plants, therefore, the earliest stages Fie. 8.— 4A, Populus monilifera,

ay fhe Higtane ak at pee Be probably spore mother-cell stage,
in the history of the microsporangia Jan. 25, 1895; x 600. B, Corylus

must be looked for during the latter americana, pollen ready for shed-
half of the growing season that pre- dang Deed) 18973. x-400.— Arter

é CHAMBERLAIN.29

cedes the season of ‘ blooming.”
This suggests that the natural end of a growing season for the
sporophyte is the attainment cf the mother-cell stage by its spo-
rangia, which is really the limit of the sporophyte in the alterna-
tion of generations; and the natural beginning of the next season
is the reduction division and the beginning of the gametophyte.
Of course such a distinction disappears in many plants whose
seasonal habits are different from those we have been consider-
ing, but it suggests a natural division of growth between seasons,
and even in annuals the mother-cell stage is a prolonged one.

32 MORPHOLOGY OF ANGIOSPERMS

The development of the microsporangia began to be de-
scribed by Nigeli ? in 1842, and was continued by Hofmeister *
in 1859—61; but the first detailed account from the standpoint
of modern morphology is that of Warming § in 1873, which has
been made the basis of all subsequent accounts. This was sup-
plemented in 1876 by Engler,® and since then numerous inves-
tigators have added extensively to the literature of the subject.

The anther at first is a homogeneous mass of small meriste-
matic cells covered by an epidermis (Fig. 9). Very early it

Fic. 9.—Development of the microsporangium. A-D, Doronicum macrophyllum: A,
transverse section of very young anther, showing primary sporogenous cell (@) and
primary parietal cell (5); B, slightly older stage; C, longitudinal section of anther in
same stage as that shown in B: J), later stage; a,sporogenous cells. £, Menyanthes
trifoliata, transverse section of a microsporangium at a still later stage showing
tapetum (¢) and microspore mother-cells (sm). F, Mentha aquatica, transverse sec
tion showing tapetum (¢) and sporogenous cells (a@).—After Warming, from Goebel’s
Outlines of Classification and Special Morphology.

becomes faintly four-lobed in cross-section, and the differentia-
tion of the vascular strand of the connective outlines the gen-
eral plan of the structure. The whole hypodermal layer of
cells, representing the outermost layer of the periblem, is prob-
ably to be regarded as archesporial in its possibilities, and one
region of it is just as likely as another, under similar eondi-
tions, to develop into actual archesporial cells. The favorable
conditions for this development, however, are under the lobes:
so that almost simultaneously with their appearance, a plate

THE MICROSPORANGIUM 33

of hypodermal cells becomes differentiated in each lobe, dis-
tinguished from the adjacent cells by their larger size, their
usual radial elongation, their larger nuclei, and their different
reaction to stains. In cross-section this plate is a single row of
cells of variable number, sometimes almost equaling in extent
the contour of the lobe, as in Mentha aquatica (Warming *) ;
sometimes consisting of four to six cells, as in Orchis maculata
(Guignard '°); sometimes three or four cells, as in Hemerocal-
lis fulva (Fullmer **) ; sometimes one or two cells, as in Conval-
laria majalis and Potamogeton foliosus (Wiegand *°); and
sometimes constantly one cell, as long known in Malvaceae and
most Compositae, and recently reported in Avena fatua by Can-
non.*° In longitudinal section the plate extends approxi-
mately the length of the anther, being a single row of cells
in case the cross-section consists of a single cell; but in Mimo-
seae the whole archesporium is reported by Rosanoff * as being a
single cell, as is also the case in Huphorbia corollata, as re-
ported by Miss Lyon.2* The general fact becomes clear, there-
fore, that an exceedingly variable amount of the hypodermal
layer may become archesporium, from nearly all of it to a single
cell; and further, that this amount usually varies within cer-
tain limits in the same species, and that the extent of the
archesporium is in no way related to the primitive or highly
specialized character of plant groups.

The subsequent divisions to the mother-cell stage usually
follow one another rapidly (Fig. 10). Following the history
of a single sporangium, the radially elongated archesporial cells
all divide equally and almost simultaneously by periclinal walls,
forming an outer layer (primary parietal,* Fig. 9, A, b) and
an inner layer (primary sporogenous,t Figs. 9, A, a, and 10,

* This has been commonly called the ‘‘primary tapetal layer,” on the
ground that the tapetum is one of its derivatives. At most only a part of the
tapetum can be derived from it, and in some cases none of the tapetum is so
derived, Besides, the tapetum is a physiological layer of variable morpho-
logical origin. The essential morphological feature of this outer sterile layer
is that it develops the wall of the embedded sporangium, and hence we have
preferred to designate it as the primary parzetal layer.

+ This is the ‘‘archesporium” of Goebel’s Outlines of Classification and of
other texts. With such an application of the term the archesporium of the
microsporangium of Angiosperms does not homologize with that of the mega-
sporangium, and is of indefinite application among the Pteridophytes. By

4 MORPHOLOGY OF ANGIOSPERMS

(aN)

A). The names used to designate these two layers indicate
their subsequent history, the former producing the wall of the
embedded sporangiun, and the latter the sporogenous tissue.

The cells of the primary parietal layer divide by periclinal
walls, so that usually a definite series of concentric parietal
layers appears (Fig. 8, 4). Walls in other directions also ex-
tend the parietal layers uniformly with the rapidly enlarging
anther. The number of parietal layers is variable, but in most
cases there are from three to five. Sometimes there are only two
layers, as in Silphium (Merrell 5) and in Quercus (Conrad **) ;
and among the Poutederiaceae Smith *? has regularly found six.
Even higher numbers have been reported, and Goebel’? (p.
368) cites Agave americana as developing eight to twelve
fibrous or endothecial layers. In Rhopalocnemis phalloides
(Balanophoraceae) Lotsy °° has shown that the sporangia of
the curious axial stamen do not organize definite parietal layers
and have no method of dehiscence, although the microspores
are fully matured.

The outermost parietal layer usually develops very differ-
ently from the others, and has been called the * endothecium.”
This name was given by Purkinje? to designate all the layers
of the dehiscing anther wall within the epidermis, which latter
he named the ‘“ exothecium.” Since in most cases the outer-
most parietal layer is the only one represented in Purkinje’s
“ endothecium,” the name has come to be restricted to it, which
seems to us unfortunate, for it should be retained in its original
application and used only in connection with the dehiseing
anther-wall. It remains true, however, that the outermost pa-
rietal layer generally becomes the endothecium, and in the fol-
lowing account this condition will be presented. If the anther
does not dehisce, the endothecial cells do not become specially
modified; bnt if the anther dehisces, the cells develop thicken-
ing bands in various ways, the position and extent of these
banded cells being directly related to the method of dehiscence
(Pie 2).

Between the outermost and innermost parietal layers there
are usually one to three “ middle lavers,” and this amount of

applying the term to the first cell or group of cells differentiated from the
ordinary vegetative cells to produce sporogenous tissue, it is easy of applica-
tion and the homologies are definite, ,

Fie. 10.—Silphium integrifolium. Longitudinal sections of microsporangia; x 520.
A, single row of archesporial cells ; in two cells division into primary sporogenous
and primary parietal cells has already taken place. 6, sporogenous and tapetal cells
sharply differentiated. (, later stage showing spore mother-cells in synapsis. D,
a tetrad (only three microspores shown) formed within the spore mother-cell.—A fter

MERRELL.28

35

36 MORPHOLOGY OF ANGIOSPERMS

variation may occur in the same wall, as noted by Coulter '?
in Ranunculus. The cells of these layers are usually tabular,
and gradually become flattened and disorganized ; but in some
cases the one or two innermost middle layers become prominent
as a part of the tapetum ; in others the outer ones may become
a part of the endothecium; and occasionally there is no dis-
organization of parietal layers.

The innermost parietal layer, as a rule, becomes part of the
tapetum, which is a jacket of nourishing cells in immediate con-
tact with the sporogenous tissue (Figs. 9,10). The tapetum has

Fie. 11.—Zostera marina. A, young microsporangium with archesporial cells shaded.
ZB, \ater stage showing tapetum derived from sporogenous cells; ¢, tapetum ; p, pollen
mother-cells; s¢, sterile cells, as shown by transverse wall. C, portions of the two
long cells resulting from the first division of the pollen mother-cell. ), portion
of a microspore showing the nuclear division that gives rise to the generative
and tube nuclei; there are six chromosomes. £, the filiform pollen grain —After
Rosenpera.’?

no definite morphological boundary or origin, but results from
pressing into special physiological service the sterile cells, of
whatever origin, contiguous to the sporogenous tissue. While one

THE MICROSPORANGIUM 37

layer of cells is the rule, the tapetum may include two or more
layers, as pointed out by Frye ** in Asclepias. The same inves-
tigator has also follow ed the or igin of that portion oF the tape-
tum next the connective
from the plate of cells im-
mediately within the arche-
sporium; and in a recent
paper Rosenberg *? — de-
scribes and figures the
much elongated archespo-
rial cells of Zostera as cut-
ting off isodiametric cells
at each end, that divide
more or less and form the
tapetum on the outer and
inner surfaces of the SpO- Fie. 12—Lemna minor. Section of microspo-
rogenous mass (Fig. Lets rangium showing some of the spore mother-
B, #). There is evidenes, siete dom an fnetoning ape
therefore, that in certain
cases the tapetum, or at least part of it, may be derived
from sterile cells cut off from the periphery of the sporog-
enous mass. Such a probability is also reported by Coul-
ter?® in Ranunculus, and by Webb** in Astilbe. Enough
is known, at least, to lead to the conclusion that any sterile
cells in contact with the sporogenous tissue assume the tape-
tal function. This is a well-known fact in connection with
sterile mother-cells, which in this sense are a part of the tape-
tum. Among the Pontederiaceae Smith?! found that the
tapetal cells, closely adherent to the mother-cells, are often
wedged among them; and in Lemna Caldwell ** observed that
the cells of the regular tapetal jacket often divide and form
groups of cells projecting deep among the mother-cells, sterile
mother-cells also disintegrating (Fig. 12); while in Symplo-
carpus Duggar ** reports that the tapetal cells become free and
“wander” among the mother-cells. It seems clear, therefore,
that the tapetum is a set of sterile cells that nourish the func-
tioning mother-cells, and that while ordinarily it is a definite
layer none of which is derived from the primary sporogenous
cells, it may include a variety of morphological elements.

As a rule, the complete organization of the tapetal jacket is

Q
Vv

(oa)

MORPHOLOGY OF ANGIOSPERMS

coincident with the mother-cell stage, but the greatest devel-
opment of the tapetal cells is during the formation of tetrads.
During this process they may increase greatly in size, this being
associated with the disorganization of the cells of one or more
of the middle layers. It is very common for the enlarged
tapetal cells, filled with food material, to become binucleate
(Fig. 10, C), and later even multinucleate, as in Typha (Schaff-
ner!7) and Lepatica (Coul-
ter?”), in the latter genus
six to thirteen nuclei hav-
ing been observed in a sin-
gle cell. At the end of the
tetrad division the tapetal
cells usually become disor-
ganized, also such of the
middle layers as have not
disorganized previously, and
. the outermost parietal layer
begins to develop the thick-
enings characteristic of the
endothecium. The fact that
the endothecium may con-
sist of additional layers of

cells has already been men-

Fic. 13.—A and D, Orchis maculata: .A, trans- tioned.
verse section of an anther with four micro-
sporangia, each showing five or six cells, :
each of which gives rise to a “ massula” as of the parietal layers the
shown in D. B,C, and £, Neottia ovata: primary sporogenous cells
B,atetrad; @,the four microspores within
the common wall dividing to form tube nu- .
cleus and generative cell; £, the division 510M. produce the mother-
completed ; two of the microspores show the cells. When division oec-
generative cell cut off by a lenticular wall.
Ax 2: Dx 240; B,C, £ x 365.—After 2
Gurenarp.t tion, so that all appearance

During the development
either directly or by divi-

curs, it is in every direc-

ot layers is lost. Perhaps
the usual case is for the primary sporogenous cells to divide two
or three times, but there are sometimes more divisions, and a
number of cases are known in which the primary sporogenous
cells, without division, become mother-cells, as has been long
known in JMalva, Datura, Mentha, and Chrysanthemum, and
recently reported for several species of Asclepiadaceae by Stras-

THE MICROSPORANGIUM 39

burger ** and by Frye.” The case of certain orchids, such as
Orchis maculata, Calanthe veratrifolia, and Neottia ovata, in-
vestigated by Guignard,’® and their allied forms, deserve special
mention, Kach primary sporogenous cell gives rise to a well-
defined mass of mother-cells known as a massula (Fig. 13, A,
D), and separated from its fellows by thicker walls.

The mother-cells and their nuclei usually increase very
much in size, and differ from the adjacent cells in their reaction
to stains. This growth is usually accompanied by a rounding
of the cells and their separation from one another, and also by
a thickening of the wall; but in many Dicotyledons (Tropaeo-
lum, Althaea, ete.) the mother-cells do not become isolated, and
remain packed closely together in the sporangium, due probably
to the tardy disorganization of the tapetum or its failure to
disorganize.

The time relations of the events described to those that form
the history of the corresponding megasporangium are exceed-
ingly variable, but the case of Astilbe, as described by Webb,**
may be taken as an illustration, especially as it probably rep-
resents an average case. The microsporangia develop rapidly,
maturing in one or two weeks, and precede the megasporangia
stage for stage. The anthers are rounded and enlarged before
the carpellary cavity is closed over; the four microsporangia
are well marked when the “ placentae” are wholly undiffer-
entiated; the tapetum is organized and the mother-cell stage
reached when the integuments have not appeared; during the
tetrad stage the integuments appear, while the microspores are
“yvounded off ” before the functional megaspore is determined.
The most extreme cases are probably certain orchids in which
pollination oceurs before ovules are formed; and oaks (Con-
rad *°), in which pollination occurs one spring and the ovules
do not develop until the next.

The case of Lemna, as reported by Caldwell,?* deserves sepa-
rate mention (Fig. 14). In the nascent anther a single hypo-
dermal group of cells appears as an archesporium and enters
upon the usual history, a wall of several layers and a broad spo-
rogenous mass being formed. <A plate of sterile cells gradually
divides this sporogenous mass into two, each of which continues
to divide as the anther increases in size. Each of these two
sporogenous masses is divided by a plate of sterile cells, so that

4

40 MORPHOLOGY OF ANGIOSPERMS

four distinct sporogenous groups are formed, each surrounded
by its own tapetum. As a result, the mature anther seems to
contain the usual four sporangia. Such a case makes the defi-
nition of a sporangium difficult. If a single archesporium is
the criterion, Lemna has a single sporangium; if a group of
mother-cells invested by a tapetum is the criterion, it has four
sporangia. The explanation probably lies in the fact that the
whole outer layer of the periblem is capable of becoming trans-

Fie. 14.—Lemna minor. Development of microsporangium and sporogenous tissue. 4
young stamen with sporogenous cells. B, two young stamens; in the one at the
left the sporogenous tissue is becoming divided by a sterile plate. (@,a more ad-
vanced stage than 2. D, a single stamen showing the four masses of sporogenous
tissue well separated by sterile plates. 4 x 1100; B,C, D x 712.—After Catp-
WELL.?3

formed into an archesporium, and that while in ordinary eases
archesporial tissue is developed in four separate regions, in
Lemna the conditions favor a more general development. To
divide a large sporogenous mass by sterile plates for better nu-
trition is too common to eall for any special remark. As for
the definition of a sporangium, it is probably not best to define
it too rigidly, but to use the term as one of convenience, From

THE MICROSPORANGIUM 41

this standpoint, there is no objection to speaking of the
tour groups of mother-cells in Lemna as four sporangia, which
have had quite an exceptional origin. The phenomenon is
too unique as yet among Angiosperms to justify any generali-
zation.

The growth of mother-cells and the enlargement of the spo-
rangial cavities usually result in reducing to a thin plate the
sterile tissue separating the two sporangial cavities on each side
of the anther. As dehiscence approaches, this plate usually
disappears, and the two sporangial cavities become fused into
a single loculus of the anther (Fig. 7). In the mature condi-
tion, therefore, such an anther contains two loculi or “ pollen-
sacs.’ While this represents the ordinary condition of the
mature anther, among the Araceae it is reported that the single
loculus of the anther is formed by the fusion of four sporan-
gial cavities, and in Sassafras it is well known that the four
remain separate. In case an anther contains only two sporan-
gia, as among <Asclepiadaceae, there is no fusion, and each
loculus is a single sporangial cavity.

The mechanism for the dehiscence of anthers is extremely
varied (Fig. 15), and needs much more investigation than it
has received. By far the most common method is by means
of a longitudinal fissure, a definite stomium developing, as in
Lilium (Fig. 7), and opening by means of the drying of the
anther-walls, the contraction of the epidermal cells being
ereater than that of the endothecial cells with their thick bands.
There is also dehiscence by a short apical fissure, as in Solanwm
and certain -Ericaceae; by a terminal pore, formed by the dis-
organization of a small portion of tissue, as in certain Erica-
ceae; by hinged valves, as in Berberis, Sassafras, and Hama-
melis; and by irregular breaking and exfoliating of superficial
tissues, as in the axial stamens of Navas. The details of these
methods, and of others, should be investigated from the stand-
point of the development of the mechanism, for such as we have
are too vague and superficial to be of much significance.

The mother-cell stage of the microsporangium is regarded
as the end of the history of the sporophyte in this direction,
chiefly because the division of the mother-cell, preceded by a
more or less prolonged rest, is a reduction division, and in con-
sequence the resulting cells have the feature most characteristic

42 MORPHOLOGY OF ANGIOSPERMS

of gametophytie tissue—namely, the reduced number of chromo-
somes (Fig. 53). With this division, therefore, the history ot
the male gametophyte begins. This line of demareation be-
tween sporophyte and gametophyte is easy to define, but does

Fie. 15.—Forms of stamens. 1, Calandrinia compressa; 2, Solanum Lycopersicum ; 8,
Galanthus nivalis; 4, Cyclamen europaeum; 5, Ramondia pyrenaica; 6, 7, Cassia
lenitiva, 8, Pyrola rotundifolia; 9, Arctostaphylos Uva-ursi; 10, A. alpina; 11,
Vaccinium uliginosum: 12, Pyrola uniflora, 13, Medinilla (after Bartion); 14,
Vaccinium Oxycoccus; 15, Caleeolaria Pavonii, 16, Tozzia alpina; 17, 18, Sibbaldia
procumbens, 19, Galeopsis angustifolia; 20, 21, Erythraca Centaureum ; 22, 28, Me-

Lo
5 ee, )

lissa officinalis, 24, 25, Calla palustris; 26, Nyctandra (after Battion); 27, 28

Globularia cordifolia; 29, 30, Theobroma Cacao, 81, Pinguicula vulgaris; 32,
Garcinia.—From Kerner’s Pflanzenleben.

’

not result in so simple a conception of the alternating genera-
tions as to begin the gametophyte with the germinating spore,
for it involves the simultaneous origin of four gametophytic
generations from the mother-cell through an intermediate divi-
sion. The claim that the reduction division must be regarded

THE MICROSPORANGIUM 43

as ushering in the gametophyte was first urged by Stras-
burger,!? whose paper closes as follows:

“ The reduction in number of the chromosomes takes place,
among the higher plants, in the mother-cells of the spores, and
it is consequently these which must be regarded as the first
term of the new generation. They assert this their true sig-
nificance in that they usually isolate themselves from cohesion
with other cells and become independent, although this inde-
pendence is only of practical utility in the case of the products
of their division—that is, of the spores. Hence the center of
eravity of the developmental processes which take place in both
miicro- and macrosporangia of Cryptogams and Phanerogams
does not lie in those cells, cell-rows, or cell-aggregates which
give rise to the sporogenous tissue and have been designated
‘archesporium’ by Goebel. The archesporium still belongs
to the sexually developed asexual generation; it is only the
spore mother-cells which initiate the new sexual generation ;
consequently the presence or absence of a well-defined arche-
sporium is not a matter to which importance should be
attached.”

LITERATURE CITED

1. Purkinse, J. E. De cellulis antherarum fibrosis nec non de gra-
norum pollinarium formis commentatio phytotomica. Vrati-
slaviae. 1830.

2. Nkceui, C. Zur Entwicklungsgeschichte des Pollens. Ziirich.
1842.

3. HormEIsTER. W. Neuere Beobachtungen iiber Embryobildung
der Phanerogamen. Jahrb. Wiss. Bot. 1: 82-188. pls. 7-10.
1858.

4, Rosanorr, 8. Zur Kenntniss des Baues und der Entwicklungs-
geschichte des Pollens der Mimoseae. Jahrb. Wiss. Bot. 4: 441-
450. pls. 31-32, 1865.

5. RoHRBACH, P. Die Samenknospe der Typhaceen. Bot. Zeit. 27:
479-480, 1869.

\6. Kaurrmann, N. Ueber die minnlichen Bliithe von Casuarina

quadrivalvis. Bull. Soc. Nat. Moscou 41: 374-382. 1869.

7”. Maanus, P. Zur Morphologie der Gattung Naias L. Bot. Zeit.
27: 769-773. 1869. Also Beitriige zur Kenntniss der Gattung
Naias L. Berlin. 1870.

| Warmuine, E. Untersuchungen tiber pollenbildende Phyllome
und Kaulome. Hanstein’s Bot. Abhandl. 2: 1-90. pls. 1-6.
1873.

io)

44

13.

14.

15.

16.

17.

18.

19.

20.

21.

22.

23.

24.

25.

26.

w
~t

MORPHOLOGY OF ANGIOSPERMS

_ Enauer, A. Beitriige zur Kenntniss der Antherenbildung der

Metaspermen. Jahrb. Wiss. Bot. 10: 275-316. pls. 20-24. 1876.

_ Gurenarp, L. Recherches sur la développement de l'anthere et

du pollen des Orchidées. Ann. Sei. Nat. Bot. VI. 14: 26-45.
pl. 2. 1882.

_ GorBeEL, C. Outlines of Classification and Special Morphology.

English translation. 1887.

_ Srraspurcer, E. The Periodic Reduction of Chromosomes in

Living Organisms. Annals of Botany 8: 281-316. 1804.

Van TIEGHEM, PH. : Observations sur la structure et la dehiscence
des anthéres des Loranthacées, ete. Bull. Soc. Bot. France 42:
363-368. 1895.

SmirH, ARMA. Abortive Flower Buds of Trillium. Bot. Gazette
22: 402-403. 1896.

CaMpBELL, D. H. A Morphological Study of Naias and Zanni-
chellia. Proc. Calif. Acad. Sci. III. 1: 1-62. pls. 1-5. 1897.

CHAMBERLAIN, C. J. Contribution to the Life History of Salix.
Bot. Gazette 23: 147-179. pls. 12-18. 1897.

ScHAFFNER, J. H. The Development of the Stamens and Carpels
of Typha latifolia. Bot. Gazette 24: 93-102. pls. 4-6. 1897.

CAMPBELL, D. H. The Development of the Flower and Embryo
in Lilaea subulata H BK. Annals of Botany 12: 1-28. pls. 1-8.
1898.

CouttsrR, J. M. Contribution to the Life History of Ranunculus.
Bot. Gazette 25: 73-88. pls. 4-7. 1898.

CHAMBERLAIN, C. J. Winter Characters of Certain Sporangia.
Bot. Gazette 25: 124-128. pl. 11. 1898.

Smitru, R. W. A Contribution to the Life History of the Ponte-
deriaceae. Bot. Gazette 25: 324-337. pls. 19-20. 1898.

Lyon, Fuorence M. A Contribution to the Life History of
Euphorbia corollata. Bot. Gazette 25: 418-426. pls. 22-24.
1898.

CALDWELL, O. W. On the Life History of Lemna minor. Bot.
Gazette 27: 37-66. figs. 59. 1899.

Fuuumer, E. L. The Development of the Microsporangia and
Microspores of Hemerocallis fulva. Bot. Gazette 28: 81-88.
pls. 7-8. 1899.

WIEGAND, kK. M. The Development of the Microsporangium and
Microspores in Convallaria and Potamogeton. Bot. Gazette 28:
328-359. pls. 24-25. 1899.

Cannon, W. A. A Morphological Study of the Flower and Em-
bryo of the Wild Oat, Avena fatua. Proce. Calif. Aead. Sei.
III. 1: 329-364. pls. 49-58, 1900.

. DuaGar, B. M. Studies in the Development of the Pollen Grain

in Symplocarpus foetidus and Peltandra undulata. Bot.
Gazette 29: 81-98. pls. 1-2. 1900.

28.

29.

THE MICROSPORANGIUM 45

MERRELL, W. D. A Contribution to the Life History of Silphium.
Bot. Gazette 29: 99-133. pls. 3-10. 1900.

ConrabD, A. H. A Contribution to the Life History of Quercus.
Bot. Gazette 29: 408-418. pls. 28-29. 1900.

. Lotsy, J.P. Rhopalocnemis phalloides Jungh., a Morphological-

systematical Study. Ann. Jard. Bot. Buitenzorg II. 2: 73-101.
pls. 8-14. 1900.

31. STRASBURGER, E. Einige Bemerkungen zu der Pollenbildung bei

Asclepias. Ber. Deutsch. Bot. Gesell. 19: 450-461. pl. 24. 1901.

2. ROSENBERG, O. Ueber die Pollenbildung von Zostera. Meddel.

Stockholms Hogsk. Bot. Inst. pp. 21. 1901.

. Frye, T. C. Development of the Pollen in some Asclepiadaceae.

Bot. Gazette 32: 325-331. pl. 18. 1901.

. WEBB, J. E. A Morphological Study of the Flower and Embryo

of Spiraea. Bot. Gazette 33: 451-460. figs. 28. 1902. For
correction of names see REHDER in Bot. Gazette 34: 246. 1902.

. SHOEMAKER, D. N. Notes on the Development of Hamamelis

virginiana L. Johns Hopkins Univ. Cire. 21: 86-87. 1902.

CHAPTER IV
THE MEGASPORANGIUM

TuE megasporangiun, just as the microsporangium, is hy-
podermal in origin, being derived from the outermost layer of
the periblem. Although strictly an embedded organ, it becomes
superticially very distinct through the growth of cells beneath
and around it, the whole structure constituting the ovule. Al
though in a strict morphological sense the ovule is more than a
megasporangium, just as the ordinary anther is more than four
microsporangia, the distinction is theoretical rather than prac-
tical, and in the following discussion will be disregarded.

Although the carpels are concerned in forming all or a part
of the encasement of the ovules, they do not always produce
them. Just as in the case of the microsporangia, and in the
same sense, there are cauline as well as foliar ovules, and the
former are much more common than are cauline microsporan-
gia. This is probably due to the fact that the ovules are much
more closely associated with the growing point of the axis than
are the microsporangia, and hence the former are much more
likely to be borne by a lateral member than the latter.

Cauline ovules are either terminal or lateral. In the former
case the apex of the axis becomes the nucellus, as is probably
true of most orthotropous ovules, certainly in Naias, Zanni-
chellia, Lilaea, Piperaceae, Juglandaceae, Polygonaceae, and
others. In the case of laterally canline ovules apical growth of
the axis may be checked, so that the lateral ovule appears to
arise ina terminal position from the bottom of the sporangial
chamber, as among the Compositae; or the apical growth may
be continued into the sporangial chamber as a dome-shaped
(Anagallis arvensis) or columnar (Sperqularia rubra, Amaran-
taceae, ete.) structure upon which numerous lateral ovules are

46

THE MEGASPORANGIUM 47

borne, giving rise to the so-called “free central placentation ”
of the older botanists. Cauline ovyles have also been reported

ah A
OND MD

Cl NAC
8 IE HI AY TA
NAS) al

Fie. 16.—A, Balanophora polyandra, with archegonium-like megasporangia; x 15.
B, B. dioica, a younger stage showing the mother-cell just after the first division;
x 200. C, B. polyandra,“ style” with a pollen-tube growing down into the “stylar
canal”; x 105. D, B. dioica, longitudinal section of a nearly ripe seed; the sus-
pensor is not shown in this section. #,a similar section through the endosperm
and embryo, showing the suspensor.—After HormeisTEr.®

in Myzodendron punctulatum by Johnson,*? and they doubtless
occur in other Santalaceae; and in Sparganium simplex, Lilaea

48 MORPHOLOGY OF ANGIOSPERMS

subulata, and certain of the Araceae by Campbell *% *% *; and
there is no doubt that numerous other cases await discovery.
It should be remembered also that in many cases of epigyny the
ovules are probably to be regard-
ed as cauline, and if these be
added to the cases already indi-
eated, it becomes evident that
cauline ovules are exceedingly
common and occur in all grades
of Angiosperms.

Tn this connection the curious
condition in Loranthaceae and
Balanophoraceae may be consid-
ered, a condition that may have
some connection with their pecul-
iar habits. In 1858 Hofmeis-
ter # ® studied various species and
outlined the prominent features

of these groups, describing and

Fie.17.—Balanophora globosa. A,nu- . . : z
cellus with mother-cell of embryo- illustrating several stages the
sac (shaded); the epidermal cells development of the archegonium-
above the mother-cell give rise to the like megasporangium, and also of
outgrowth resembling the neck of an = a
the endosperm and embryo of

archegonium. J£, later stage in which
the mother-cell has divided intotwo Balanophoraceae (Fig. 16), and

: eae - ; ¢ 5
celle, both of which “vei often de olag the puazlne “mamelon*” in
velop into embryo-sacs”; x 166,— oy ;

After Lorsy.48 Loranthaceae. Subsequent inves-

tigators have in the main con-
firmed and extended this work, the most important modifi-
‘ation being in the interpretation of the embryo; and even
here Hofmeister’s figures are nearly identical with those
of the most recent papers (cf. Fig. 16 with Fig. 107). In
1882 Treub?* deseribed the development of the pistil of
Loranthus sphaerocarpus (Fig. 19). A structure (‘* mame-
jon”) arises from the bottom of each of the three or four
sporangial chambers and grows until it completely fills it,
and in this structure hypodermal archesporia appear and
develop megaspores in the usual way. It is a fair question
whether the “ mamelon” is a growth of the axis, whose ovules,
represented by separate archesporia, are mechanically hindered
from any superficial development; or whether it is an ovule

THE MEGASPORANGIUM 49

without an integument, in which there are several archesporia.
Hofmeister favored the latter view, while Treub inclined to the
former, as his explanation of it as a fusion of rudimentary
ovules and placentas would seem to indicate. In 1883 Treub 1”
discovered exactly the same structure in Loranthus pentandrus.
In 1895 the same investigator *? described Balanophora elon-
gata as having no ovule or placenta. In 1896 this was con-
firmed by Van Tieghem** for B. indica; and in 1899 by
Lotsy ** for B. globosa (Fig. 17). Lotsy claims that in B.
globosa there are no flowers, carpels, placenta, or ovules; but
that a hypodermal cell in a protuberance of the floral axis gives
rise to the embryo-sac, while
the epidermal cells over it de-
velop a long, style-like organ
resembling the neck of an
archegonium. Hofmeister de-
scribes and figures the pollen-
tube of B. polyandra as grow-
ing down into this “ stylar
canal,” as he called it (Fig.
16,C). It would appear from
the figures that the “ protu-
berance of the floral axis” is
a megasporangium without in-
teguments, and that the so-
ealled “ style” is a remarkable
outgrowth of the nucellus.
The pollen-grains, as figured
by Hofmeister, therefore, come
in contact with the nucellus,
as in Gymnosperms. In this
connection attention may be
called to the remarkable beak yye, 13.—Fuphorbia corollata. Longitudi-
developed by the nucellus of nal section showing an excessive pro-
Euphorbia corollata as de- oo pte Oar
sevibed by Miss Lyon *? (Fig. ,

18), a beak which suggests the same general tendency of the nu-
cellus which has reached such an extreme expression in Balano-
phora. The investigation of Rhopalocnemis phalloides ( Balano-
phoraceae) by Lotsy,°? however, as well as the case of Balano-

50 MORPHOLOGY OF ANGIOSPERMS
phora, suggests the explanation. Lotsy finds that the enlarged tip
of the flower axis soon completely fills the cavity of the ovary,
and that one or more hypodermal
cells of this axis form the mega-
spores (Fig. 20). This is exactly
the case of Loranthus, and suggests
that in the allied Balanophora the
same “mamelon” is present, but
with no carpellary investment, the
naked nucellus (as the “ mamelon”
would seem to be in this case) de-
A veloping the remarkable neck-like
outgrowth of sterile tissue. In both
families it seems certain that the
megasporangia are cauline.

Foliar ovules are related to the
carpels in a variety of ways. By far

the most common position is for the
ovules to arise in a line along each
side of one of the two prominent vas-
cular bundles of the carpel, a very
common position for the sporangia
of ferns. In the older morphology
this line was thought to represent the
abutting margins of the infolded car-
pellary leaf, and hence such ovules
were called “marginal.” In fact,
this double line of ovules, and the
Fie. 19.—Loranthus sphacrocarpus. dehiscence of many carpels along it,

A, longitudinal section ofa young seemed to the supporters of meta-

flower showing the “mamelon” ‘ aa
(m); x 25. B, longitudinal sec- morphosis to prove the fohar nature
tion of a “mamelon” at a later of the carpel. As might be expected
stage showing two hypodermal ;
archesporial cells; x 300.—After .
Trevp.!8 ferns, there are eases in which ovules

from the behavior of sporangia in

arise withont such close connection
with a prominent vaseular bundle. For example, in Butomus,
Nymphaea, Nuphar, Obolaria, Bartonia, and many species of
Gentiana, the ovules arise from the whole inner surface of the
earpel. In the older terminology these were called ‘ super-
ficial ” ovules, and associated with them, curiously enough, were

THE MEGASPORANGIUM 51

the occasional cases in which the ovules arise from the other vas-
cular bundle (the “ midrib” of the infolded leaf theory), as in
Brasenia, Cabomba, and Astrocarpus (Eichler,’ 2: 17). Ac-
cording to Warming’ a third category is necessary to include
such cases as Zannichellia, Ranunculus, and Sedum, in which
he says the ovules are “ basal or axillary.”

The general conclusion seems evident that ovules may arise
from any free surface within the cavity of the ovary, whether
it be morphologically carpel or axis; and further, that if the
cavity of the ovary becomes obliterated by the enlarged tip of

(ZL)
PELs
le)
(oJ

roo
Seca
sey

eo
Sas:

es
SOccs
(2)

RII
io,
ieeeesoeaes
,o)

G6:60
Caceorsere

Fic. 20.—Rhopalocnemis phalloides. A, longitudinal section through the “mamelon”
before the appearance of archesporial cells. 6, later stage showing the two mega-
spore mother-cells which develop directly into embryo-sacs. x 116.—After Lotsy.5?

the axis, as probable in Loranthaceae and Balanophoraceae,
megasporangia arise from the hypodermal cells of the axis
without the definite organization of ovules.

The morphological nature of the ovule was much discussed
by the older morphologists. According to the theory of meta-
morphosis it was necessary to interpret it as a transformation
of some one or more of the vegetative members. The most
prevalent view was that it is a transformed leaf-bud arising
from the margin of the carpellary leaf, as in the well-known
case of Bryophyllum; and Hofmeister claimed that the ovule
of Orchis is a trichome because it arises from a single epidermal

MORPHOLOGY OF ANGIOSPERMS

bo

5

cell. When cauline ovules came to notice, Schleiden, End-
licher, and others took the extreme position that all ovules are
cauline, even those evidently parietal upon carpels. This view
was opposed by Van Tieghem,® Celakovsky,” and especially
by Warming.t° The last-mentioned paper is noteworthy for
its presentation of the origin and development of the ovule, as
well as for its discussion of its morphology. These writers
maintained that the ovule is always foliar in origin, and their
explanations of cauline ovules are interesting on account of
their ingenuity. This view was also maintained by Eichler
in his Bliithendiagramme, where an historical résuine of the
whole subject may be found. The most interesting feature of
the whole discussion, however, is the persistent idea that ovules
could not be both foliar and cauline. These last observers, hav-
ing established the foliar origin, disproved the bud character
of ovules, since the members of leaf-buds arise in acropetal
succession, while the nucellus and integuments are basipetal.
It was urged that the ovule is a transformed leaf-lobe or leaf-
outgrowth, and that this view homologized them with the spo-
rangia of ferns. This was a decided step in advance, and it
only remained to abandon the doctrine of metamorphosis, and
to see that the ovules (sporangia) hold no necessary relation to
either leaf or stem, but are themselves long-established and
independent members of the plant body, with a history that
antedates that of either stem or leaf.

The length of time from the beginning of megasporangia to
their maturity is very indefinitely known, as most investigators
do not seem to have kept such a record. It must be extremely
variable, as in the case of the microsporangia, and related to
the seasonal habit of the plant. In Salix and Populus Cham-
berlaim *° found that the megaspore mother-cells are not distin-
guished until the renewal of growth in the spring, although the
microsporangia pass the winter in the mother-cell stage; and
this lateness of development may be usual in the megaspore
series. Enough eases have been observed, however, to show that
a much earlier development may often occur. For example, in
Acer rubrum Mottier 27 discovered the mother-cell stage in
March or earlier, the indication being that this is the winter
condition; Chamberlain °° found the four megaspores of T'ril-
lium recurvatum fully formed early in April, when the plants

THE MEGASPORANGIUM 53

were not more than 5 centimeters high, and the embryo-sac of
Hepatica ready for fertilization while the ground was still
frozen; we have seen embryo-sacs of Epigaeca ready for fertil-
ization in the autumn, pollination probably occurring the fol-
lowing spring; and Schaffner °° has found that in Lrythronium
the archesporial cell begins to enlarge about the first of October
and nuclear changes occur, and that by the first of December the
nucleus is very large and the mother-cell stage reached, which
persists until early spring. The subject should be investigated
especially in connection with vernal herbs and early blooming
shrubs and trees.

The details of the development of the ovule have been ad-
mirably given by Warming ?° and Strasburger,!? supplement-
ing and correcting the earlier observations of Hofmeister,* ®
and the literature since has grown so extensively that full cita-
tion is impossible (Fig. 21). At first the epidermis of the mem-
ber upon which the ovule is to appear is even, and in the hypo-
dermal layer the archesporium may or may not be evident. A
shght protuberance is developed by cell-divisions, which are
usually only radial in the epidermal layer, resulting in a more
extended plate of cells; but in the hypodermal layer they are
variable, resulting in a mass of tissue, or In many cases in but
a single axial row of cells. In any event, the protuberance
becomes more and more prominent and constitutes the nucellus
of the nascent ovule.

After the nucellus has become prominent, an annular out-
erowth begins at its base, and with greater or less rapidity
develops into the inner and often only integument, in most
cases overtopping the nucellus (Fig. 3, 2). In case there is an
outer integument, its annular primordiuin becomes visible soon
after the inner integument is well under way (Fig. 21). If the
aril he placed in this category, it has been observed that this
third integument arises much later than the other two, usually
after fertilization, as in Asphodelus, Aloe, Nymphaea, Podo-
phyllum, Euonymus, Celastrus, Myristica, ete., although in all
these cases its point of origin does not seem to be well estab-
lished. Disregarding the aril, two integuments seem to be the
rule among Monocotyledons, the only recorded exception we
have noted being Crinum, although, doubtless, there are others.
Two integuments prevail among the Archichlamydeae also, the

Fie. 21.—Lilium philadelphicum. A, ovule before the appearance of integuments,
showing a single hypodermal archesporial cell which is also the megaspore mother-
cell. B, beginning of inner integument. C, beginning of outer integument. LD, £,

later stages. F, G, the ovule anatropous and the megaspore germinating. x 175.

54

THE MEGASPORANGIUM 55

Umbelliferae being the most notable exception. On the other
hand, a single integument is characteristic of the ovules of the
Sympetalae, as well as of the Umbelliferae, and some other
Archichlamydeae, such as species of Ranunculus, Leguminosae,
etc., the integument being very massive and in comparison with
the very small nucellus constituting the bulk of the ovule.
There seems to be every indication that two integuments are
characteristic of the ovules of the more primitive Angiosperms ;
that they persist among Monocotyledons even among the most
highly specialized fanuhes; but that among Dicotyledons they
are replaced in the higher groups by the single massive integu-
ment. The fact that the single integument is more massive
even than both integuments when there are two suggests that it
represents two integuments in the sense that their primordia
are no longer differentiated. This is very far from meaning
that two integuments have fused to form the single one, but
that a single integument is developed by the same region that
in other cases produces two.

Certain exceptional cases in the development of integu-
ments may be noted. Among the Loranthaceae and Balano-
phoraceae no integuments are formed; and the same claim is
made by Chauveaud ?* °° for Cynanchum (Asclepiadaceae),
perhaps to be explained by Asclepias (Frye °°), in which the
integument might be mistaken for part of a naked nucellus.
The same claim is made for Santalaceae, and it may be true
of most of them; but in Myzodendron punctulatum Johnson **
has described a’ single-layered integument that does not cover
the free end of the embryo-sac. This suggests an abortion
of the integument, which in other members of the family
may not have been recognized or may even have been sup-
pressed. The ovule of Houstonta is said by Lloyd ®! to have
no integument. The ovule of Mippuris long had the reputation
of having no integument, as reported by ‘Schleiden,! Unger,”
and Schacht.2 In 1880, however, Fischer '° in reinvestigating
it discovered that a single integument is formed, but closes over
the nucellus so tightly as to give the appearance of a naked
nucellus. Oliver 2! discovered exactly the same behavior in
his new genus Trapella, except that the integument is very
massive. The same thing has also been observed by Murbeck *7

in the parthenogenetic Alchemilla alpina, in which the single
5

56 MORPHOLOGY OF ANGIOSPERMS

integument so completely coalesces with the nucellus and closes
the micropyle that the ovule resembles a naked nucellus. Zin-
ger * observed that the massive inner integument in Canna-
bineae is completely coalescent with the thick outer one over the
apex of the nucellus, and the micropylar canal becomes entirely
closed by the development of tissue. In cases of chalazogamy
and persistent parthenogenesis such behavior of the integu-
ments may be expected, as well as in other cases whose habits
do not suggest it.

In most cases, the ovule does not merely become distinct
from the surface of the member that produces it, but is borne
upon a stalk-lke base or funiculus. It is generally stated that

Fie. 22.—Forms of ovules (diagrammatic). 4, orthotropous; B, anatropous; C, cam-
pylotropous ; 7, micropyle; e, embryo-sac ; , nucellus; c, chalaza; (7, funiculus.—
After Pranti in Engler and Prantl’s Nat. Pilanzentad,

the ovules of Gramineae have no funiculus, but it would be im-
possible to draw an exact line between its presence and absence.

The direction of growth of the ovule seems to be related
to the orientation of the micropyle in reference to the pollen-
tube. Mirbel gave to the resulting forms the names ortho-
tropous, campylotropous, and anatropous (Fig. 22). In the
first case the growth continues without the development of any
curvature, a fact generally true of terminal ecauline ovules.
Orthotropous ovules are quite common, being found among
Monocotyledons in the Restiaceae, Eriocaulace eae, Xyridaceae,
certain Araceae, Commelinaceae, ete.: and among Dicotyledons
in the Piperaceae, Urticaceae, Polygonaceae, Cistaceac, ete.
These are relatively primitive families of Monoeotyledons and
Archichlamydeae, and confirm the natural impression that the

THE MEGASPORANGIUM 57

original angiospermous ovules were straight. The campylotro-
pous ovule, in which the whole body of the ovule curves, is the
rarest type, among Monocotyledons characterizing the Grami-
neae, Scitamineae, ete., and among Dicotyledons the Cheno-
podiaceae, Caryophylaceae, Cruciferae, Capparidaceae, Reseda-
ceae, ete. These families are more or less specialized members
of their alliances, and none of them belong to the Sympetalae.
By far the most common form of ovule is the anatropous, and
although it is extensively displayed among Monocotyledons and
Archichlamydeae, it is present almost without exception among
the Sympetalae, and may be regarded as the most highly spe-
cialized type of ovule. In its development an anatropous ovule
is at first straight or nearly so, but very early develops a curva-
ture at a level with the origin of the first or only integument.
As the integuments grow the curvature increases, and usually
before the outer integument is complete the nucellus is inverted
against the funiculus (Fig. 21). For this reason, in anatropous
ovules with two integuments the outer one is not developed on
the side toward the funiculus. In abnormal material of Salix
petiolaris both anatropous and orthotropous ovules have been
observed in the same ovary (Fig. 6).

The archesporium, as in the microsporangia, is recognized
by the increasing size and the different reaction to stains of one
or more hypodermal cells. Doubtless all of the hypodermal
cells are potentially archesporial, and there is reason for be-
heving that the deeper cells of the nucellus, most of which are
probably derivatives from the original hypodermal layer, may
be also. In the vast majority of cases, however, only cells of
the hypodermal layer show those changes that are character-
istic of archesporial cells. It is not always easy to determine
just how many hypodermal cells are to be included in the ar-
chesporium, for there is often complete gradation from cells
with the size and staining reaction of undoubted archesporial
cells to those showing neither increase in size nor the character-
istic staining reaction. This is to be expected in case all the
hypodermal cells are potentially archesporial, and there is no
definite point in its history when such a cell ceases to be merely
hypodermal and becomes clearly archesporial. For this reason,
the number of cells recorded as constituting the archesporium
in many plants can not be regarded as precise, but as approxi-

58 MORPHOLOGY OF ANGIOSPERMS

mate. The prevailing habit, however, is to limit the arche-
sporium to the single hypodermal cell that terminates the axial
row of the nucellus. This seems to have resulted in the more

~
SY
na N
188
a

pone 3

Fie. 23.—Longitudinal sections of ovules showing multicellular archesporia. A, B,
Astilbe japonica, x 550; after Wenn.8? CO, Salix glaucophylla, x 600; after Cnam-
BERLAIN.SS 1), Rosa livida, x 224; after SrraspuraER)s £, Alehemilla alpina,
x 275; after Mursrox.6? F, Callipeltis cueullaria; after Liuoyp.! G, Quercus
velutina, x 720; after Conran.53

highly specialized groups in reducing the nucellus within
the epidermis to this axial row, as Lilium, many Orehida-
ceae (Dumée**), Lobeliaeeae (Marshall-Ward 1+), Rubiaceae
(Lloyd §'), Compositae, and many other sympetalous groups.
In such eases the nucellus in longitudinal section shows only
three rows of cells. ,

It is of interest to note the recorded cases in which the
archesporium is said to consist of more than a single cell (Fig.
23). In 1879 Strasburger}% described the several-celled ar-
chesporium of Rosa livida, and in 1880 Fischer 15 reported a
similar archesporium in Geum, Sanguisorba, Agrimonia, Ru-

THE MEGASPORANGIUM 59

bus, and Cydonia, indicating that this is the prevailing tend-
ency among the Rosaceae. In 1882 Guignard!* added Erio-
botrya to the list, and in 1901 Murbeck °7 foynd an archesporial
group in Alchemilla alpina. Recently, however, Péchoutre °°
has made a general survey of the Rosaceae, and in all of the
fourteen genera studied, well distributed among the tribes, there
was found a many-celled archesporium, showing a remarkable
persistence of this character throughout a large family. Among
the closely allied Saxifragaceae also, Webb °° has found in
Astilbe this same type of archesporium.

In 1891 Treub ** published his account of Casuarina, re-
porting that the archesporium is a group of hypodermal cells,
and that the derived sporogenous tissue forms a large central
mass within the nucellus (Fig. 24). The account and the fig-

UNG
DY aun

CH

{|

Fie. 24.— Casuarina. Longitudinal sections of nucellus. 4, section showing two pri-
mary sporogenous cells (shaded); x 190. JB, later stage showing extensive sporog-
enous tissue; x 190. ©, pollen-tube (with heavier walls) among the elongated
sterile megaspores ; x 67. D, portion of nucellus at a much earlier stage than C,
showing numerous megaspore mother-cells ; x 157.—After TrEvp.23

ures suggest that all of the sporogenous tissue may not be
derived from the hypodermal layer. In 1894 Miss Benson *
discovered that a several-celled archesporium is present in Fa-

60 MORPHOLOGY OF ANGIOSPERMS

gus, Castanea, Corylus, and Carpinus, in the last-mentioned
form finding a large central mass of sporogenous tissue. Later,
Chamberlain 2® found that there are sometimes two or three
cells or even six in the archesporium of Salix, and occasionally
five or six in that of Populus tremuloides. Then Conrad *?
described the archesporium of Quercus velutina as consisting
of a mass of twenty to sixty or even more cells, all of which are
megaspores (Fig. 23). The archesporia of Casuarina, Car-
pinus, and Quercus are certainly not all hypodermal, like those
of the Rosaceae, in which the resemblance to the development
of the microsporangia is striking. In Juglans cordiformis
Karsten ®t has also found an extensive sporogenous tissue. A
several-celled or even a many-celled archesporium, therefore,
seems to be a frequently expressed tendency among the Amen-
tiferae,* although it is by no means uncommon among them
to find the archesporium consisting of a single cell, as in A/nus
and Betula.

Among the Ranunculaceae great irregularity in the num-
ber of archesporial cells is found even in a single species.
Guignard 1" first found that in Clematis cirrhosa the archespo-
rium is sometimes two-celled; and in 1895 Mottier *° stated
that the archesporium of Delphinium tricorne is sometimes
more than one-celled, that of Ranunculus abortivus one or two-
celled, that of Caltha palustris two to five-celled, and that of
Anemonella thalictroides probably many-celled. Later Coul-
ter *8 found the archesporial cells of several species of Ranun-
culus varying in number from one to thirteen (Fig. 25), and
the several-celled archesporium of //elleborus cupreus is ta-
miliar. It is evident, therefore, that the Ranunculaceae, while
ordinarily producing a one-celled archesporium, show a strong
tendency to an increase in the number of cells.

These three groups, Amentiferae, Ranunculaceae, and Rosa-
ceae, are recognized as among the more primitive members
of the Archichlamydeae, and the temptation is strong to con-
clude that the many-celled archesporium is a primitive feature
of the Dieotyledons. This may be true in a very general
sense, for no large groups have shown such a general tendency,
but account must be taken of the same phenomenon in other

* Used in this connection only as a term of convenience to include several
of the more primitive orders of Arechichlamydeae.

THE MEGASPORANGIUM 61

groups. Fischer ?° describes a several-celled archesporium in
Helianthemum, Guignard '* an occasional two-celled archespo-
rium in Capsella, and Treub'* a two-celled archesporium in
Loranthus and one of four or five cells in Visewm, while it has
long been known that Thesium has a several-celled archespo-
rimn. More to the point, however, is the occurrence of a several-
celled archesporium among the Asclepiadaceae (Frye °*), the
Rubiaceae (Lloyd * +) (Fig. 23), and the Compositae. In the
latter family Ward '* describes an occasional archesporium of
three cells in Pyrethrum balsaminatum, Mottier 2° found an
occasional two-celled archesporium in Senecio aureus, and the

Fie. 25.—Ranunculus septentrionalis. Longitudinal sections of nucellus, x 400. A,
eight-celled archesporium. J, later stage showing germinating megaspores with
two and four nuclei.—After CouLTER.%

several-celled archesporium of Chrysanthemum Leucanthemum
is well known.

It is somewhat remarkable that among the Monocotyledons
there is no record of an archesporium of more than one cell
except in the case of Ornithogalum pyrenaicum, which Guig-
nard+* reports to have an archesporium of two cells, only
one of which gets beyond the archesporial stage; and the pos-
sible case of Lilium candidum, in which Bernard *! reports two
embryo-sacs. We have also seen two preparations of L. phila-
delphicum, one showing three archesporial cells and the other
five.

62 MORPHOLOGY OF ANGIOSPERMS

The archesporial cells behave as do those of the microspo-
rangium, and in ease the archesporium is a plate of cells, the
resemblance is striking. In the large majority of cases, how-
ever, the archesporinn is a single cell, and often by transverse
division it gives rise to a primary parietal cell and a primary
sporogenous cell (Fig. 26). That the former cell, or plate of
cells, as it is in the case of a several-celled archesporium, repre-
sents the primary parietal layer of the microsporangium seems
clear. In recognition of this fact
Strasburger called it the ‘“ tapetal
cell,” but for reasons given under
the microsporangium we shall call it
the parietal cell—that is, a cell that
develops in part the wall of the em-
bedded sporangium. Mottier °° has
reported a very peculhar case in Ari-
saema, im which the single archespo-
rial cell divides by anticlinal walls
into three or four cells, each of which
then cuts off a parietal cell. Just
how far this is exceptional behavior
remains to be seen, but it intro-
duces an interesting problem as to
the application of the term archespo-
rium.

Fie. 26.—Salix glaucophylla. Lon- The behavior of the primary
gitudinal sections of nucellus, parietal cell is exceedingly varied.
. 631. A, single hypodermal sine oe 5 .
archenporialicall (a), Bi arche. OD extreme case is for a series of

sporial cell has given rise to pri-_ periclinal divisions to occur, result-
mary parietal cell (¢) and pri-
mary sporogenous cell (m).— ‘ i
After CHAMBERLAIN.%® corresponding to the parietal layers

of the microsporangium. In ease
there is a plate of archesporial cells the radial rows of parietal
cells are very conspicuous, as in the Rosaceae and many of the
Amentiferae (Figs. 23, B, D, E). In other eases the parietal
rows become lost by the formation of anticlinal walls. If
the mother-cell broadens rapidly, the first divisions of the pri-
mary parietal cell may be anticlinal, followed by periclinal
divisions, as in Ruta graveolens (Guignard 17) and Potamoge-
ton foliosus (Wiegand **), The deep-placing of the sporoge-

ing in a long row of parietal cells,

THE MEGASPORANGIUM 63

nous cells beneath parietal tissue occurs in Potamegeton (Wie-
gand,°* Holferty **), Z'riticum (Koernicke 3*), Ayraphis
(Vesque **), Triglochin (Vesque !*), Lysichiton (Campbell +7),
Rosaceae, Saxifragaceae, many Leguminosae (as Lupinus, Cer-
cis, Acacia), Euphorbiaceae, Cuphea (Guignard 37), Fuchsia
(Vesque’*), Mesembrianthemum (Guignard 17), and doubtless
many other Monocotyledons and Archichlamydeae.

From a conspicuous development of parietal tissue there
is a complete gradation to its entire suppression. A few peri-
clinal divisions of the parietal cells may occur or none at all.
Sometimes in case the periclinal divisions have been abandoned,
one or more anticlinal divisions may be induced by the broad-
ening of the mother-cell, as the single periclinal division in
Typha (Schaffner *°) and Lemna (Caldwell #*), and the series
of such divisions in Convallaria (Wiegand **) and Butomus
(Ward ?*),

The gradation toward the suppression of parietal tissue
is further illustrated in cases where the primary parietal cell
divides or not in the same species, as in the grass Cornuco-
pie (Guignard 17), Pontederiaceae (Smith *°), Yucca: (Guig-
nard 17), and Thalictrum (Overton *®). The next stage is rep-
resented by the constant failure of the parietal cell to divide,
as in Alyssum (Miss Riddle **) and Limnocharis (Hall ®’).
The last case is of special interest from the fact that in the
cutting off of the primary parietal cell no wall is formed, and
the cell speedily disappears through the growth of the mother-
cell.

The transition from an incomplete and ephemeral primary
parietal cell to none at all is natural, and this final stage, in
which there is complete suppression of the parietal tissue, has
been reached by many plants. It may be of interest to consider
how far this condition has been reached by the great groups.

Among Monocotyledons the suppression of parietal tissue
occurs in all the higher families, but it is usually associated
also with the greater or less development of this tissue. Among
Gramineae, Cannon °° reports Avena fatua as having no parie-
tal cell, although other Gramineae are known to possess it, and
in Triticum (WKoernicke **) it develops an extensive tissue.
Among Commelinaceae, Guignard 17 records Commelina stricta
as without a parietal cell, and Strasburger?* figures T'rade-

6+ MORPHOLOGY OF ANGIOSPERMS

scantia virginica as having one. Among Liliaceae, Allium,
Hemerocallis, Lilium, Erythronium, and Tricyrtis have no pa-
rietal cell; and Convallaria, Funkia, Scilla, Ornithogalum, Tril-
lium, and Yucca are known to have one. Among Ividaceae, the
only records we have been able to find are those of Sisyrinchium
iridifolium (Strasburger 1°) and Iris stylosa (Guignard 17), in
neither of which is there a parietal cell; but it would be very
unsafe to predicate this condition for the whole family. Among
the Cannaceae, Guignard 17 reports Canna indica as sometimes
having a parietal cell and sometimes not, but Wiegand ** finds
in it only an abundant parietal tissue; and the other Scitami-
neae are reported by Humphrey *? with parietal tissue. Among
Orchidaceae, Gymnadenia conopsea (Strasburger ?*) and Or-
chis pallens (Goebel,?’ p. 391) were long ago reported as with-
out a parietal cell, but recently Dumée,** examining a number
of genera and species of orchids, reports them all as having
parietal cells. This record probably fairly represents the con-
dition of the parietal tissue among Monocotyledons. It indi-
cates a general tendency to suppress it, which has been success-
ful in certain members of the higher and more specialized
families.

Among the Archichlamydeae approximately the same con-
<ition prevails. The Ranunculaceae exhibit a surprisingly uni-
form suppression of the parietal tissue, this condition having
been found in Anemone, Caltha, Clematis, Delphinium, Myo-
surus, and Ranunculus (Fig. 27); while in Aquilegia a parietal
cell may or may not appear. Only Helleborus (Guignard 17)
and Thalictrum (Overton *®) have thus far been reported as
having a parietal cell, and this may or may not divide. It is
to be noted that in Delphinium, Caltha, and Jeffersonia the
absence of parietal tissue is compensated for by numerous peri-
clinal and anticlinal divisions of the overlying epidermal cells;
and in the Balanophoraceae this epidermal growth reaches so
remarkable a development that Treub at first called it a stvle.
The same development is seen in ITippuris (Fischer ™), in which
the apical epidermal cell divides by anticlinal and periclinal
walls and forms a small, wedge-shaped cushion that prevents
the micropyle from being entirely obliterated by the closing
in of the integument. Among the Berberidaceae, Jeffersonia
( Andrews #1) has no parietal cell, and Mahonia indica (Guig-

THE MEGASPORANGIUM 65

nard‘*) has. Among the Papaveraceae, Papaver orientale
(Vesque !*) has no parietal cell. Among Cruciferae, Capsella
(Guignard 17) has no parietal cell, but Alysswm (Miss Rid-
dle **) has one that does not divide. Among the Leguminosae,
Orobus angustifolius (Guignard 1°) is the only one recorded as
without a parietal cell; and among the Umbelliferae, Siwm
has no parietal cell, but in the allied Araliaceae a parietal cell
is cut off (Ducamp ®*). That Loranthaceae and Balanophora-
ceae have no parietal tissue is probably only a part of the ex-
tensive modification of their megasporangia. It is perhaps
noteworthy that the suppression of parietal tissue among Ar-

\ ia
=| (=>) eee
VGN ZAG IEA
Fie. 27.— Ranunculus multifidus. Longitudinal sections of nucellus, x 475. A, single
archesporial cell (shaded) which is also the megaspore mother-cell, no parietal cell
being formed; two of the epidermal cells above the archesporial cell show peri-
clinal divisions. -B, second division of the megaspore mother-cell, by which four

megaspores are being formed.—After CouLTEr.%

chichlamydeae is most extensively displayed by the Ranuncu-
laceae and its allies, rather than by the more specialized groups ;
but no generalization is safe until some knowledge of the gen-
eral conditions among the Umbelliferae and other high groups
of the Archichlamydeae is available.

The strongest argument that suppression of the parietal
tissue of the megasporangium is a strong tendency among An-
giosperms is that this condition is universal among the Sym-
petalae so far as investigated.

The primary sporogenous cells do not divide to increase
the number of sporogenous cells, so that in the megasporangium

66 MORPHOLOGY OF ANGIOSPERMS

of Angiosperms the primary sporogenous cell is the mother-cell.
The only possible exception to this is the case of such sporog-
enous masses as occur in the ovules of Casuarina (Treub ~),
Carpinus (Miss Benson **), and Quercus (Conrad °°). If the
whole:sporogenous mass in these forms is derived from a hypo-
dermal archesporium, then of course the primary sporogenous
cells divide to form additional sporogenous cells. But if all
the sporogenous tissue is an archesporium, in this case con-
tributed to by cells deeper than the hypodermal layer, the pri
mary sporogenous cells do not divide, nor do all the archesporial
cells give rise to parietal cells. In any event, the cells of the
completed sporogenous mass, Whether archesporial or not, are
mother-cells.

The history of the development of the microsporangia and
megasporangia is strikingly similar. In both cases the arche-
sporium is hypodermal; in the microsporangium it is usually a
plate of cells and exceptionally a single cell, while in the mega-
sporangium it is usually a single cell and exceptionally a plate
of cells. In both each archesporial cell divides by a periclinal
wall, cutting off a peripheral parietal cell that takes part in
developing a sporangium wall of a variable number of layers.
In the development of the megasporangium, however, there is
a strong tendency to suppress the wall layers, probably as of
no significance or even a hindrance in the process of fertiliza-
tion. While in the microsporangium the primary sporogenous
cells often divide a few times before the mother-cell stage is
reached, this is by no means always the case; and although in
the meg:

sporangium the primary sporogenous cells usually do
not divide to form mother-cells, this is probably not always true.
In both sporangia the mother-cells, reached by the same
sequence of events, are recognized by the fact that their division
is the reduction division. —

It is at this point that the history of the megasporangium
closes, for the reduction division is the beginning of the female
gametophyte (see p. 41).

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AO.

MORPHOLOGY OF ANGIOSPERMS

Outver, F. W. On the Structure, Development, and Affinities of
Trapella, a New Genus of Pedalineae. Annals of Botany 2:
75-115. pls. 5-9. 1888.

Jounson, T. The Nursing of the Embryo and some Other Points
in Myzodendron punctulatum Banks et Sol. Annals of Bot-
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Trevus, M. Sur les Casuarinées et leur place dans le systeme natu-
rel. Ann. Jard. Bot. Buitenzorg 10: 145-231. pls. 12-32. 1891.

. CHAUVEAUD, G. L. Sur la fécondation dans les cas de polyembry-

onie. Compt. Rend. 114: 504. 1892.

. Mottirer, D. M. On the Development of the Embryo-sac of

Arisaema triphyllum. Bot. Gazette 17: 258-260. pl. 18. 1892.
On the Embryo-sac and Embryo of Senecio aureus L.
Bot. Gazette 18: 245-253. pls. 27-29. 1893.

. Development of the Embryo-sac in Acer rubrum. Bot.
Gazette 18: 375-377. pl. 34. 1898.

. BENSON, MARGARET. Contributions to the Embryology of the

Amentiferae. I. Trans. Linn. Soc. London 8: 409-424. pls. 67-72.
1894.

. TREUB, M. L’organe femelle et lapogamie du Balanophora elon-

gata. Ann. Jard. Bot. Buitenzorg 15: 1-22. pls. 1-8. 1898.

. Mortier, D. M. Contributions to the Embryology of the Ranun-

culaceae. Bot. Gazette 20: 241-248, 296-304. pls. 17-20. 1895.

. ANDREWS, F.M. Development of the Embryo-sac of Jeffersonia

diphylla. Bot. Gazette 20: 423-424. pl. 28. 1895.

. Humpurey, J. E. The Development of the Seed in Scitamineae.

Annals of Botany 10: 1-40. pls. 1-4. 1896.

3. KOERNICKE, M. Untersuchungen iiber die Entstehung und Ent-

wickelung der Sexualorgane von Triticum mit besonderer Be-
riicksichtigung der Kerntheilung. Verhandl. Naturhist, Ver.
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- VAN TIEGHEM, PH. Sur l’organisation florale des Balanophora-

cées. Bull. Soc. Bot. France 48: 295-309. 1896.

. CHAMBERLAIN, C. J. Contribution to the Life History of Salix.

Bot. Gazette 28: 147-179. pls. 12-18. 1897.

. SCHAFFNER, J. H. The Development of the Stamens and Carpels

of Typha latifolia, Bot. Gazette 24: 93-102. pls. 4-6. 1897.

. CAMPBELL, D. H. The Development of the Flower and Embryo

in Lilaea subulata HBK. Annals of Botany 12: 1-28. pls. 1-3.
1898.

38. COULTER, J. M. Contribution to the Life History of Ranunculus.

Bot. Gazette 25: 73-88. pls. J-7. 1898.

CHAMBERLAIN, C. J. Winter Characters of Certain Sporangia.
Bot. Gazette 25: 124-128. pl. 11. 1898. .
SMITH, R. W. A Contribution to the Life History of the Pontede-

naceae, Bot. Gazette 25: 324-337. pls. 19-20. 1898.

41,

43.

44.

49.

50.

51.

53.

54.

THE MEGASPORANGIUM 69

Lyon, FLoRENCE May. A Contribution to the Life History of
Euphorbia corollata. Bot. Gazette 25: 418-426. pls. 22-24.
1898.

. RIDDLE, Lumina C. The Embryology of Alyssum. Bot. Gazette

26: 314-324. pls. 26-28. 1898.

ZINGER, N. Beitraége zur Kenntniss der weiblichen Bliithen und
Inflorescenzen bei Cannabineen. Flora 85: 189-253. pls. 6-10.
1898.

DUMEE et MaLinvaup. Un Vicia nouveau pour le flore francaise.
Bull. Soc. Bot. France 46: (Sess. Extraord.) xxx-xxxii, 263-266.
pls. 2. 1899.

. Luoyp, F. E. The Comparative Embryology of the Rubiaceae.

Bull. Torr. Bot. Club 28: 1-25. pls. 1-3. 1899.

3. CALDWELL, O. W. On the Life History of Lemna minor. Bot.

Gazette 27: 37-66. figs. 59. 1899.

. CAMPBELL, D. H. Notes on the Structure of the Embryo-sac in

Sparganium and Lysichiton. Bot. Gazette 27: 153-166. pl. 1.
1899.

. Lotsy, J. P. Balanophora globosa Jungh. Eine wenigstens Grt-

lich-verwittwete Pflanze. Ann. Jard. Bot. Buitenzorg II. 1: 174-
186. pls. 26-29. 1899.

CAMPBELL, D.H. Studies on the Araceae. Annals of Botany 14:
1-25. pls. 1-3. 1900.

Cannon, W. A. <A Morphological Study of the Flower and
Embryo of the Wild Oat, Avena fatua. Proc. Calif. Acad. Sci.
III. 1: 329-364. pls. 49-53. 1900.

BERNARD, C. H. Recherches sur les spheres attractives chez.
Lilium candidum, ete. Jour. Botanique 14: 118-124, 177-188,
206-212. pls. 4-5. 1900.

Lotsy, J.P. Rhopalocnemis phalloides Jungh., a Morphological-
systematical Study. Ann. Jard. Bot. Buitenzorg II. 2: 73-101.
pls. 3-14. 1900.

Conrap, A. H. A Contribution to the Life History of Quercus.
Bot. Gazette 29: 408-418. pls. 28-29. 1900.

Wincanp, K. The Development of the Embryo-sac in some
Monocotyledonous Plants. Bot. Gazette 30: 25-47. pls. 6-7.
1900.

55. Hotrerty, G.M. Ovule and Embryo of Potamogeton natans.

Bot. Gazette 81: 339-346. pls. 2-3. 1901.

| Scuarrner, J. H. A Contribution to the Life History and Cytol-

ogy of Erythronium. Bot. Gazette 31: 369-387. pls. 4-9. 1901.

- Mureeck. §. Parthenogenetische Embryobildung in der Gattung

Alchemilla. Lunds Univ. Arsskrift. 836: No. 7, pp. 46. pls. 6.
1901: Bot. Zeit. 59: 129. 1901.

Hau, J.G. An Embryological Study of Limnocharis emargi-

nata. Bot. Gazette 33: 214-219. pl. 9. 1902.

MORPHOLOGY OF ANGIOSPERMS

. OVERTON, J. B. Parthenogenesis in Thalictrum purpurascens.

Bot. Gazette 83: 363-375. pls. 12-13. 1902.

. Wess, J. E. A Morphological Study of the Flower and Embryo

of Spiraea. Bot. Gazette 33: 451-460. figs. 28. 1902. For cor-
rection of name see REHDER in Bot. Gazette 34: 246. 1902.

il. Luoyp, F. BE. The Comparative Embryology of the Rubiaceae.

Mem. Torr. Bot. Club 8: 27-112. pls. 8-15. 1902.

62. Ducamp, L. Recherches sur ’embryogénie des Araliacées. Ann.

Sei. Nat. Bot. VIIL 15: 311-402. pls. 6-13. 1902.

3. PEcHouTRE, F. Contribution a l’étude du développement de

lovule et de le graine des Rosacées. Aun. Sci. Nat. Bot. VIII.
16: 1-158. figs. 166. 1902.

. Karsten, G. Ueber die Entwicklung der weiblichen Bliithen bei

999

einigen Juglandaceen. Flora 90: 316-333. pl. 12. 1902.

. CHAUVEAUD, G. L. De le reproduction chez le dompte-venin.

Diss. Paris. 1902.

. Frye, T.C. A Morphological Study of Certain Asclepiadaceae,

Bot. Gazette 34: 389-413. pls. 13-15. 1902.

CHAPTER V
THE FEMALE GAMETOPHYTE

Tue literature relating to the female gametophyte of Angio-
sperms is so extensive that one can not hope to compass all of
its details. We have selected for critical examination numerous
examples, well distributed throughout the great groups, and the
conclusions from these must fairly represent the present state
of knowledge. Even in these cases it would be hopeless to
attempt the presentation of all the details to which attention
has been called, and only those will be considered that seem
most significant. There is a prevalent impression that with
very few exceptions the history of the female gametophyte is
rigidly uniform, but an examination of the literature reveals
considerable variation. This impression has doubtless arisen
from the fact that the standard texts have almost uniformly
selected a single type of history for description.

The important literature of the subject dates from Hof-
meister,’ 2 whose work was supplemented and corrected by
Warming,? Vesque,* Strasburger,® Fischer,® Marshall-Ward,®
Treub and Mellink,!° Guignard,'!1* and others. During the
last twenty years numerous investigators have added to the lit-
erature, and much of their work will be referred to later.

It was stated in the previous chapter that we regard the
history of the female gametophyte as beginning with the divi-
sion of the mother-cell. The ordinary product of this division
is an axial row of cells whose morphological nature was long
a subject of discussion (Figs. 28, 29). By many they were
regarded as mother-cells that do not divide, but at present there
is general agreement with the view, stated hy Overton °° (p.
172) in 1893, that they are megaspores. This means that the
usual row of four cells produced by the mother-cell represents

6 71

72 MORPHOLOGY OF ANGIOSPERMS

the tetrad usually formed by the microspore mother-cell. The
first mitosis in the megaspore mother-cell always shows the

Fie. 28.— Trillium recurvatum, Longitudinal sections of nucellus, showing some early
stages in the development of the female gametophyte; x 500. 4, megaspore mother-
cell; nucleus shows six chromosomes, the gametophyte number. Z, first division
of nucleus of mother-cell, (C) second division of nucleus of mother-cell ; mitosis
nearer chalaza much further advanced than that at micropylar end. D, germina-
tion of megaspore nearest chalaza; the other three megaspores represented only by
a dense, Shapeless mass.

THE FEMALE GAMETOPHYTE 73

reduced number of chromosomes, and this is true whether a row
of two, three, or four megaspores is to be produced, or the
mother-cell is to develop directly into the embryo-sac, as in
Lilium. In such forms as Lilium the second mitosis also corre-
sponds in all essential details with the second division that is to
result in a row of four megaspores. The third mitosis differs

Fie. 29.—A, Canna indica; axial row of four megaspores, the innermost one beginning
to germinate and the other three disintegrating ; after Wircanp.£° B, Hichhornia
crassipes: portion of nucellus showing four megaspores, the innermost one germi-
nating, and the other three, which are not separated by walls, disintegrating;
«1100; after Smirn.53

from the usual sporophytic mitosis only in the reduced number
of chromosomes (Miss Sargant,? Strasburger,’? Juel 8). Not
only do the first two divisions agree in the various types, but
they correspond minutely with the two divisions with which
the microspore mother-cell gives rise to the tetrad. That the
megaspores do not occur in tetrahedral or bilateral arrange-
ment does not involve their morphological nature, for in the

74 MORPHOLOGY OF ANGIOSPERMS

microspores are formed in rows of four as well as tetrahedrally,
while in Asclepias (Strasburger,’® Frye °’) the microspores
constantly appear in rows of
four (Fig. 58); and in the
pollen mother-cells of Zos-
tera (Rosenberg **) the four
elongated microspores — lie
side by side in the same
plane. Nor is it a criterion
of a tetrad that all of its

spores shall mature, for in

. 80.2 tsia ji ica. Longitudinal - 88 ae
Fie 4, Fa sia japonica ongi . a 2 Carex acuta (Juel ah ( Fig.
section of nucellus showing two tetrads ; : 2. ae
x175. £B, similar section of Aralia race- 59) only one spore of the

mosa,in which the nucellus bears a strong tetrad functions, a habit to
resemblance to 5 Misrosporangran, x 340 he observed alsacamione the
—After Duoamp.4 5
Pteridophytes, as in Mar-
silea and Azolla. Even the rare case of more than four mega-
spores in a row is met by the occasional occurrence of more than
four microspores in the pollen mother-cells of Hemerocallis fulva
(Juel,®° Fullmer *) and of Huphorbia corollata (Miss Lyon **)
(Fig. 60). The usual tetrad arrangement, however, is not lack-
ing among megaspores, as observed by Ducamp 1° in Fatsia
japonica (Fig. 30), in which after the mother-cell had divided
transversely the two daughter-cells were observed to divide longi-
tudinally ; and in one preparation, in which two mother-cells had
thus divided, the nucellus looked very much like an ordinary spo-
rangium. In another case the middle cell of a row of three had
divided longitudinally. The parallel seems still more striking
when microspores germinate like megaspores, even reaching the
stage with eight free nuclei, as observed by Némee ** in the petal-
oid anthers of [Tyacinthus orientalis, whose microspores some-

pollen mother-cells of Typha (Schaffner *?) (Fig. 57) the

times show three successive mitoses, giving rise to four nuclei at
each end of the pollen-erain (Fig. 31). Even the formation of
three cells at one end, and the wandering of one polar nucleus
toward the middle were observed, although fusion did not oeeur.
Némee did not hesitate to homologize these divisions with those
occurring in the embryo-sac. There seems to be no longer any
reasonable objection to the view that this row of cells, whioee
formation is initiated by the reduetion division, is the homo-

THE FEMALE GAMETOPHYTE 75

logue of the tetrad formed by the microspore mother-cell. The
most recent suggestion as to the nature of the embryo-sac is that
made by Atkinson,!°! who claims that in the ovule there do not
exist spores “in the sense in which they are represented in the
Pteridophytes, or in the microspores of the Spermatophytes,”
but that the angiospermous embryo-sac arises directly from
nucellar tissue without the intervention of spores. As spores
are not needed for distribution they are “cut out of the cycle
of development, and the embryo-sac or gametophyte arises
directly from the tissue of the sporophyte.”

In our own judgment it seems clear that the cells in question
are morphologically megaspores, and if so it would follow that
the natural tendency of the megaspore mother-cell is to form a
tetrad. The fact that the spores form a row may be due to the

Fie. 31.—Hyacinthus orientalis. Abnormal germination of microspores in petaloid
anthers. A, the microspore has formed a sac-like tube showing definite polarity ;
B,ashort pollen-tube resembling an embryo-sac at the third nuclear division ; the
heavy line below represents the thick wall of the pollen-grain; C,a later stage,
showing four nuclei at each end of the sac-like pollen-tube.—After Nemec.

pressure of the surrounding tissue, there being no opportunity
for early isolation and rounding off as in microsporangia. It
may be of interest to note that sometimes after the first divi-
sion of the mother-cell the outer daughter-cell divides by an
anticlinal rather than a periclinal wall, as observed in Butomus

76 MORPHOLOGY OF ANGIOSPERMS

(Marshall-Ward *), Jeffersonia (Andrews **), and Potamoge-
ton (Holferty °7). In the ease of Cynomorium (Juel1?"), the
two cells resulting from the first division of the mother-cell are
very unequal, the micropylar one being the smaller. This
smaller cell divides longitudinally and the larger one trans-
versely. Transitions to this condition in the formation of
oblique walls sometimes occur, as in Delphinium (Mottier *°),
The case of Fatsia japonica has been referred to above. As
already indicated, the completion of a tetrad is by no means
always attained, for there is every gradation between a row
of four megaspores and an undividing mother-cell that func-
tions directly as a megaspore. The explanation of this tend-
ency to shorten the megaspore series is probably connected
with the fact that only one megaspore of the tetrad functions.
The number of megaspores formed by the mother-cell has been
reported for very many plants, but the records are by no means
of equal value. The reasons for this are obvious. One is that
the sterile axial cells of the nucellus often simulate megaspores,
so that too large a number might easily be reported, and great
care is necessary to distinguish them; and another is that the
technique of the earlier observers did not always permit cer-
tainty. By far the most important source of inaccuracy, how-
ever, is the hasty examination of a great number of forms by
a single investigator. Two megaspores might be reported,
when the same ovule collected a few hours later might have
shown four megaspores. As a consequence, much of the avail-
able data can be used only in a very general way as indicating
tendencies of groups.

Among the Monocotyledons, about one-third of those investi-
gated are reported as forming complete tetrads, in another
third the mother-cell does not divide, while the remaining forms
show every intergradation. Although one might expect the
complete tetrads to be characteristic of the more primitive
Monocotyledons, and the undividing mother-cell characteristic
of the higher families, there is as yet no such evidence, both
conditions oeeurring in all grades of Monoeotyledons.

The greatest variability is found among the Liliaceae, possi-
bly because more of the species have been investigated (compare
Fig. 28 with Figs. 35 and 36). For example, without attempt-
ing to inelude all the recorded eases, in Hemerocallis (Stras-

THE FEMALE GAMETOPHYTE rie

burger ®), Trillium (Chamberlain *?), and Galtonia (Schnie-
wind-Thies °°) four megaspores are reported, although in the
last genus only two may appear; in Anthericum (Strasbur-
ger”), and Tricyrtis and Yucca (Guignard!*) three; in Alli-
wm (Strasburger®), and Agraphis and Ornithogalum (Guig-
nard**) two; while in Lilium, Fritillaria, Funkia, Tulipa,
Convallaria (Wiegand *°), and Brytheoimun (Schaar Be)
the mother-cell cee not divide. It may be of interest to note
the records of other investigators in reference to some of these
genera. For example, Ikeda1°° reports four megaspores in
Tricyrtis hirta, and Vesque* three in Hemerocallis, Allium,
and Convallaria.

Among the more primitive aquatic families, Zostera (Ro-
senberg**) and Potamogeton (Wiegand,** Holferty 97) have
three or four megaspores; in J'ypha (Schaffner *°) there is no
division of the mother-cell; and among the Alismaceae, Alisma
(Schaffner **) and Limnocharis (Hall?) have an undividing
mother-cell, while Butomus (Ward ®) has three and sometimes
four megaspores.

Among the Gramineae the complete tetrad is common
(Fischer *), but Guignard +” reports only two megaspores in
Cornucopiae.

Among the Araceae Mottier °* reports two megaspores in
Arisaema, and Campbell ** the same number in Dieffenbachia,
while in the allied Lemna (Caldwell ®*) the mother-cell does not
divide.

Among the Pontederiaceae (Smith **) there are four mega-
spores, while Guignard 12 reports only two in Commelina.

Among the higher families, Narcissus (Guignard!*) has
an undividing mother-cell; Zris (Guignard !*) has three mega-
spores (Vesque* reports four), and T'ritonia and Sisyrinchium
(Strasburger®) four; the Scitamineae have three or four,
excepting Costus (Humphrey *°), in which the mother-cell does
not divide; while the orchids Gymnadenia (Strasburger *) and
Orchis (Vesque *) have a row of three or four megaspores.

That detailed study would show that many of these numbers
are not constant is indicated in several instances. In Arisaema,
in which two megaspores are customary, Mottier 27 found one
case in which the transverse wall did not form, the elongated
mother-cell appearing with a nucleus at each end; while in Dief-

78 MORPHOLOGY OF ANGIOSPERMS

fenbachia, of the same family, Campbell *® states that the inner
one of the two cells may divide, forming a row of three mega-
spores. Among the Pontederiaceae, Sinith 53 found great varia-
tion in the development of the megaspores. While sometimes
the row of four is formed by equal successive divisions, it is
more common for the mother-cell to elongate greatly, with its
nucleus near the micropylar end. In this position two succes-
sive and rapid divisions of the nucleus occur in any order or
direction, and four usually naked cells are the result, the inner-
most being much the largest and speedily obliterating the others,
becoming the functioning megaspore (Fig. 29, B). In Avena
fatua, Cannon §° found that four cells are formed; or the
mother-cell may contain four nuclei without any cell walls, the
three outermost disappearing, the innermost forming the nu-
cleus of the functioning megaspore. In Potamogeton foliosus,
Wiegand °° found that the second divisions in forming the row
of four are not accompanied by walls, and Holferty °* found in
Potamogeton natans that the outermost wall may not appear
even when there is nuclear division. Such cases emphasize the
fact that there may often be the greatest variation in the devel-
opment of megaspores, and that a number reported for a species
by a hasty observer should not be regarded as a fixed one, or
even possibly the customary one.

The only generalization that seems to be safe in reference
to the Monocotyledons, aside from the fact of their great irregu-
larity, is that more of them than of the Dicotyledons have
reached the condition of an undividing mother-cell.

Among the Archichlamydeae, nearly all the species investi-
gated have three or four megaspores, and both of these numbers
are represented in almost every family in which more than one
species has been studied. Upon the whole, however, a row of
three megaspores seems to be more common than one of four.
For example, among the Ranunculaceae, of eleven genera stud-
ied only four have been reported as having four megaspores, and
in all of these cases three megaspores have also been observed.
The four genera referred to are Aquilegia, in which five mega-
spores were also observed, Delphinium, Ranunculus (Fie. 27),
and Thalictrum, and in each of these eases different observers
have given different numbers. In Caltha, which ordinarily has
three megaspores, Mottier 3° occasionally found nuclear divi-

THE FEMALE GAMETOPHYTE 79

sion, unaccompanied by a wall, in the outermost cell of the row
of three. There is every evidence that in this family the inner
cell of the first division always divides, and the other one may
or may not divide, resulting in three or four megaspores.
Almost the only exception to three or four megaspores, in case
the mother-cell divides, noted among Archichlamydeae is J/s-
cum articulatum (Treub!), in which the four or five mother-
cells divide only once, the inner cell becoming the functional
megaspore.

This same variation is found in at least twenty other fam-
ihes of the Archichlamydeae. Probably the most variable case
recorded is that of Salix glaucophylla (Chamberlain **), in
which there may be three megaspores, or two, or the mother-cell
may not divide.

The few cases among Archichlamydeae in which the mother-
cells are not known to divide are three genera of Piperaceae
(Peperomia, Piper, Heckeria) investigated by Johnson,7 114
but the allied Saururus (Johnson §7) has a row of three mega-
spores; Alchemilla alpina (Murbeck ®*), but this is associated
with the occurrence of a large mass of archesporial tissue; the
Cactaceae (D’Hubert #*); and at least Sium cicutaefolium
among the Umbelliferae. In Juglans cordiformis Karsten 11°
finds great variability, the mother-cell functioning directly as the
megaspore or giving rise to a row of three or four megaspores,
the two outer ones never functioning, the two inner ones appar-
ently having an equal chance, and in many cases developing two
sacs. Among the Araliaceae also, Ducamp 1!” reports that the
mother-cell becomes the megaspore directly or produces a row of
three or four megaspores. The same is true of the Balanophora-
ceae, as shown by Lotsy §* in Rhopalocnemis, and by Chodat
and Bernard ** in /Telosis; but the conditions in this family are
so peculiar that the phenomenon does not seem significant. In
Casuarina (Treub*°) (Fig. 24) and Quercus (Conrad 7*), in
which there is a large mass of sporogenous cells, there is no
division of mother-cells to form spores. The behavior of the
numerous mother-cells of Casuarina is remarkable, a certain
number developing as embryo-saes, a larger number remaining
sterile and becoming very much elongated, and still others be-
coming tracheid-like cells.

It is apparent, therefore, that among the Archichlamydeae

80 MORPHOLOGY OF ANGIOSPERMS

the mother-cell very rarely fails to divide, but that there is a
strong tendency to suppress one of the divisions and form a
row of three megaspores.

Among the Sympetalae the complete tetrad appears with
remarkable uniformity. This is associated with a very small
nucellus, most frequently only the epidermal layer investing
the tetrad row, and the suggestion is evident that there may be
some causal relation between these two facts. Occasionally,
however, one of the divisions is suppressed, and a row of
three megaspores is the result, the only cases we have found
being Vaccintwm and Lycium (Vesque+), Lobelia (Marshall-
Ward), Lonicera and Nicotiana (Guignard 1"), and Trapella
and Sarcodes (Oliver 7!» 74). Among the Rubiaceae Lloyd 1%
reports that while each mother-cell forms a tetrad there are
usually no walls (Fig. 33), as in Avena (Cannon 8°) and Eich-
hornia (Smith **). Among the Verbenaceae Treub 14 reports
that in Avicennia officinalis the mother-cell does not divide; in
Aphyllon uniflorum Miss Smith1°? reports that the mother-
cell does not divide, although IXoch!® figures a row of four
megaspores in Orobanche; in the parthenogenetic Antennaria
alpina Juel ™* finds that the mother-cell does not divide, how-
ever, in A. dioica, in which fertilization regularly occurs, a
row of four megaspores is formed. Undoubtedly more numer-
ous exceptions will be found, but the evidence seems clear that
the complete row of four megaspores is almost universally pres-
ent among the Sympetalae.

As has been stated, the reduction in the number of chromo-
somes occurs during the first mitosis in the meg: aspore-mother-
cell, whether a row of four, or three, or two megaspores is to
be formed, or the mother-cell is to function direct ly as a mega-
spore. In Lilium, the first described form in which the oe
cell does not divide to form megaspores, the beginning of :
cell-plate is clearly visible in the spindle during the first mito-
sis, and at the second mitosis there is also a rudimentary cell-
plate. Since the other evtological characters of these two mito-
ses are identical with the first two mitoses in forms that have
the row of four megaspores, it might be suggested that the
rudimentary plate is a survival, indicating that the ancestors
of Lilium once produced the row of four, and making Lilium
in this respeet a specialized rather than a primitive form. This

THE FEMALE GAMETOPHYTE 81

seems reasonable, but it must be noted that the rudimentary
plate occurs also at the third mitosis, and so may be a reminis-
cence of a much more remote ancestry with cellular prothalla.

In connection with the reduction division it is of interest
to note the number of chromosomes found among Angiosperms.
The following table, arranged in the Engler sequence of fami-
lies, although more extensive than any hitherto published,
far from complete. The numbers in parentheses were inferred
rather than actually counted:

The Number of Chromosomes recorded for Certain Angiosperms

| CHROMOSOME NUMBERS.
PLANT. ‘ Observer. Year.

eng | Sporophyte.
LOSLETH MATING 0 cee eee es 6 12 Rosenberg” | 1901
IN GUAS GI OF on cschetsict ch asvereaats aes 6 12 Guignard™ 1899
Triticwm vulgare... ...se.ee- 8 (16) Overton 8 1893
aa nee ater ye 8 16 Koernicke # | 1896
TrOGOSCONTG:: csi cieueee bas 0s 12 mostly 16 Strasburger ”° | 1888
Bichhornia crasstpes.......00. 16 (82) Smith 1898
Pontederia cordatd..........4. 8 16 ay 1898
Chlorophytum Sternbergianum 12* 2 Strasburger ° | 1888
Funkia Stieboldiana........... 24 (48) Strasburger 7 | 1900
Alli wan Jistulosum Leal NaS 8 16 Strasburger 7° | 1888
e SUNT D o aris Ane econ ae aes 8 (16) Guignard * 1891
CM GENO seas cemannen (8) 16 Schaffner 1898
DUM as hdew sais niet eens 12 mostly 16 Strasburger ?° | 1888
ff Pane: lain Gt htare dose ah 12 24 Guignard 16 1884
a Seine ak Os 12 24 Sargant * 1896
“ eandidum.... 1... 0005. 12 24 Strasburger ?° | 1888
a CROCOUI: 3 ce cen aeaynue & 12 24 1888
philadelphicum ....... 12 24 Schaffner # 1897
ue LGTUNUM. 2.0 cee er eee 12 24 ea 1897
Fr itillar ia impertalis......... 12 24 Strasburger 7° he
Meleagris.......56. 12 24 Guignard 26 1891
Tulipa Gesneriand.......00.5. 8 16 Schn.-Thies® | 1901
Erythronium americanum. .... 12 24 Schaffner® | 1901
Galtonia candicans........... 8 16 or less Sehn.-Thies ® | 1901
Scilla non-scripta.......0.. 65. 8 (16) Overton *§ —_| 1893
BUOUP LCT so )s hic coe eseersos 8 variably 8-16 Sehn.-Thies® | 1901
Muscart neglectum Sochag Sae a Gata 24 48 | Strasburger 2° 1888
Cc ‘onvaltar Wh MOIAUS.. 6 are ees 16? more than 16 a | 1888
Liege Urea 18 (36) Wiegand * | 1900
Trillium grandiflorum ooo... 6 12 Atkinson * | 1899
recUurvalUM ...ccceees 6 12 The authors, | 1902
Deucojum vernumd. .. 0.002.000 12 (24) Overton 78 | 1893
Alstroemeria ... sce cece ceeeee 8 mostly 16 | Strasburger2° | 1888
my PSH ACEO... cee 8 16 Guignard*6 | 1891
TRUS SQUALENS vases tiie 8 ea te Rae |) 2 24 Strasburger 7 | 1900
CONNGTRONCI 5,059 gence es 3 6 Wiegand ® 1900
Cypripedium barbatum........ 16 32 Str; asburger 2 } 1888

* One anther constantly 14.

82 MORPHOLOGY OF ANGIOSPERMS

The Number of Chromosomes—Continued

CHROMOSOME NUMBERS.

PLANT. ' | Observer. Year.

Gameter —sporophyte,
OV CRIS: MASCULD:. 2 ie arses aan 16 (32) Strasburger ”° | 1888
Himantoglossum hircinum..... 16 (32) oe 1888
Gymnadenta COnOpsed......... 16 (32) as 1888
Listera ovat... ee. cee. ey 16 (32) Guignard *6 1891
Neottia nidus-avis........0.6% 16 (32) : 1891
Nymphaea alba oo... eee eee 32 (64) Guignard °° 1898
i He oS raniiea soreyseers oecers 48 (96) Strasburger ™ | 1900
Ceratophyllum submersum..... 12 24 | Strasburger 1902
Aconitum Napellus........... 12 (24) | Overton 4 1893
FTelleborus foetidus... 0.0.2... 12 24 Strasburger *? 1888
: Sti kane eeneee: 12 mostly 16 Strasburger *° | 1894
Paeonia spectabilis ... 0.2.0... 12 (24) Overton ** 1893
Podophyllum peltatum........ 8 16 Mottier * 1895
Alehemilla alpina *. 2... ...04. 32 32 Murbeck * 1901
Asclepias Cornutt. ........000% 10 20 Strasburger | 1901
ee (UDCTOSO 5.5 sec caw. 10 20 Frye 1901
PAS NOP UNG cro rac cates at @ Siete ee eye 12 24 Lloyd 1% 1902
OP UCUOTON ON. ma hieis iene Breen cs 10 20 ss | 1902
Antennarta alpina*.......... 40-50 40-50 Juel * | 1900
as DMOUE, can cies 12-14 counted 20 os | 1900
Silphium integrifolium ....... 8 (16) Merrell 7 | 1900
us laciniatum.......... 8 16+ | Land *} 1900

It is evident from the table that Strasburger and Guignard
were pioneers in this work and that they still remain the most
active contributors. It is of interest to note that when atten-
tion was first directed to this subject, the number of chromo-
somes reported for the sporophyte, while exceeding that of the
gametophyte, was not precisely twice that number. The sub-
ject is one of great difficulty, and doubtless the countings of
competent investigators have often been influenced by their
theories, while their followers have been content too often with
confirming a reported number. Variations from the character-
istie number are numerous. In the gametophyte the number
of chromosomes in the antipodals is frequently irregular, with
a tendency to higher numbers; but an explanation may be found
in the irregular nuclear divisions whieh present some of the
characters of amitosis (Miss Sargant 41). Variations are even
more frequent in the sporophyte, but it is well known that
mitoses are frequently irregular, and it is easy to imagine that
a chromosome may fail to split or that an unequal distribu-

* Parthenogenetic. } More than 16, probably 24, in endosperm.

THE FEMALE GAMETOPHYTE 83

tion to the daughter nuclei may occur. The high numbers
reported for the endosperm are doubtless to be explained by
the triple fusion.

In the great majority of cases the gametophyte number has
been counted only in the mother-cells, and the sporophyte num-
ber in the tissues of the ovule or young embryo. Still, ocea-
sional counts throughout the entire life-history show that the
reduced number that occurs in the division of the mother-cell
is maintained up to the time of fertilization, whether the inter-
ral be short, as in Angiosperms, where only from three to five
nuclear divisions intervene between reduction and_ fertiliza-
tion, or long, as in the liverworts, where the gametophyte is the
more permanent generation and the sporophyte is a compara-
tively temporary structure.

Why the number of chromosomes should be so constant, and
why a reduction in number should take place, are the most
important questions in this connection. The constancy of the
numbers has led many to believe that the chromosome is a
permanent organ of the nucleus, just as the latter is a perma-
nent organ of the cell; but no one would assign such a reason
for the constant recurrence of six stamens in a lily. There is
other evidence in favor of the individuality of the chromosomes,
but it does not seem to be sufticient. The physiological advan-
tages are evident, for the constancy in number enables each
parent to transmit an equal number of chromosomes to the off-
spring, and the reduction prevents the constant geometrical
increase in the number of chromosomes which would otherwise
occur. Strasburger °° says: “‘ The morphological cause of the
reduction in the number of the chromosomes and of their equal-
ity in number in the sexual cells is, in my opinion, phylogenetic.
I look upon these facts as indicating a return to the original
generation from which, after it had attained sexual differentia-
tion, offspring were developed having the double number of
chromosomes. Thus the reduction by one-half of the number
of chromosomes in the sexual cells is not the outcome of a
eradually evolved process of reduction, but rather it is the reap-
pearance of the primitive number of chromosomes as it existed
in the nuclei of the generation in which sexual differentiation
first took place. . . . The reduction in the number of chromo-
somes takes place, in the higher plants, in the mother-cells of

84 MORPHOLOGY OF ANGIOSPERMS

the spores, and it is consequently these which must be regarded
as the first term of the new generation.”

In case the mother-cell divides, only the inermost mega-
spore functions, its growth involving the digestion and absorp-
tion of the other megaspores, as well as more or less of the sur-
rounding sterile tissue. Ordinarily the elongating megaspore
encroaches upon the others until they become merely a cap upon

but among the Ranunculaceae Guignard}* found in Cle-
matis and LHelleborus, and Mottier 2° in Delphinium, that the
nucellus elongates so rapidly that the sterile megaspores are
not crowded into a cap, but their disorganization leaves a nar-
row cavity. The same thing occurs in Jeffersonia, as shown
by Andrews,?* and doubtless among many other Archichla-
mydeae. The known exceptions to the functioning of the inner-
most megaspore are so few that they deserve special mention,
as possibly indicating some peculiar condition.

Among the Monocotyledons, Agraphis (Scilla) and Dieffen-
bachta are the only exceptions we have noted. In the former,
Treub and Mellink?° observed that the outer one of the two
megaspores becomes the embryo-sac, but the inner one also de-
velops a sac to the four-nucleate stage, an observation later con-
firmed by Guignard !? for other species of the genus. In Agra-
phis nutans Vesque * observed the uppermost of a row of three
megaspores functioning, but the ordinary divisions within the
embryo-sac, up to four nuclei, were also observed in two or
even all of the megaspores. The same observer also reports
that in Yueca gloriosa all four megaspores show sac tendencies,
while in Uvularia each spore in a row of two developed an
embryo-sac to the four-nucleate condition. In Dieffenbachia,
Campbell ® says that the mother-cell divides very unequally,
the outer one being the larger and developing the embryo-sac.
In Galtonia candicans (Liliaceae) Schniewind-Thies ® has ob-
served an interesting transition to the condition of Lilium and
similar forms. The mother-cell usually gives rise to a row of
four megaspores, but occasionally only two spores appear, one
of which may pass over directly into the embryo-sae.

Among the Archich: amydeae, in Juglans cordiformis (Kar-
sten!®). the two ehalazal Inegaspores may both develop em-
bryo-sacs; the outermost megaspore of the row often functions
in Stellaria Holostea (Vesque*) and in Rosa, and sometimes

THE FEMALE GAMETOPHYTE 8d

in the latter the two outer begin the formation of embryo-sacs ;
and in Hriobotrya Guignard ?* found that while ordinarily the
innermost megaspore of three functions, the middle or the outer
oue may torm the embryo-sac, and even all three may begin its
formation. The same author?! also reports great irregularity
in Acacia, in some species the innermost of four megaspores
functioning, in others the next outer one, and in still others
the middle one of a row of three. In
Loranthus also, Treub 1® finds that the
outermost megaspore of three persist-
ently functions. Among the Aralia-
ceae (Ducamp?!*) usually the inner-
most of four megaspores functions, but
occasionally one of the middle cells
may become the embryo-sac. Such
cases serve to emphasize the megaspore
character of all the cells of the row.
Among the Sympetalae, the only
well-established exception is that of
Trapella, in which Oliver *! finds that
the outermost of four megaspores func-
tions, and in one case the next cell,
while the innermost megaspore devel- os
ops the remarkable haustorium (Fig. Fre. 32. — Zrapella sinensis,

32). In Asclepias tuberosa, although Ovule some time after fer-
i tilization: m, micropyle; s,

synergids ; sp, suspensor; 4,

the innermost of the row of four mega-

spores ordinarily functions, Frye 1! embryo; e, endosperm; 2,
has observed cases in which the outer- vascular bundle; ¢, two long

‘ cells resulting from the lon-
most megaspore functions, and others eibudinal divisionofthelow-
in which the two innermost develop ermost megaspore of a row

of four; x 100.—After Ox1-

: SEN SS Pe i Te 4s, oe ;
together; while Vesque* reports that = 7)

in Salvia pratensis the outermost of

the four megaspores functions. In Crucianella (Lloyd °°)
all four megaspores, which in this case are not separated by
cell-walls, may begin to germinate (Fig. 33). Guignard?”
also includes Pyrethrum as among the forms whose outer-
most megaspore functions, but it needs further investigation.
It should be noted in this connection that when a row of four
megaspores is to be formed, the nucleus nearest the chalaza al-
most invariably shows a more advanced stage in mitosis than

56 MORPHOLOGY OF ANGIOSPERMS

the nucleus nearer the micropyle, as shown for Trillium in
Fie. 28. Hence the megaspore at the chalazal end of a row
is formed a little earlier than the one at the micropylar end.

Fic. 33.—Crucianella macrostachya. A, four-nucleate embryo-sac and three disintegra-
ting megaspores ; the four megaspores of this axial row not separated by cell-walls.
ZB, axial row of four megaspores which are not separated by cell-walls; each mega-
spore has germinated and is in the binucleate stage. C, an embryo-sac (with two
nuclei) and four sets of megaspores ; the megaspores of one set germinating.—Atter
Lioyp.196

A still more important reason for the selection of the chalazal
megaspore is doubtless its more immediate relation to the nutri-
tive supples coming through the base of the ovule, a fact which
may also account for the earlier mitosis at the chalazal end of
the row.

In case there is more than one mother-cell, two or more
megaspores may begin the development of embryo-saes, which
may even attain the fertilization stage, but in almost every case
one embryo-sae prevails over the others. Among the Monocoty-
ledons two embryo-saes are reported as sometimes occurring in
Lilium candidum (Bernard ®*); and in Agraphis (Vesque,!
Guignard !?) and Uvpularia (Vesque *), as referred to above,
all of the two or three megaspores of the single row develop
embryo-saes to the four-nueleate stage. Among the Archiehla-
mydeae, five to eight sacs begin to develop in Loranthus

THE FEMALE GAMETOPHYTE 87

(Treub*°) and in Casuarina (Treub **); in Viscum articula-
tum (Treub’™) all of the four or five megaspores reach the
two-nucleate stage; in Salix (Chamberlain **) occasionally two
embryo-sacs are found in the fertilization stage; in Fagus,
Corylus, and Carpinus (Miss Benson *) two or more completed
sacs have been observed; in Juglans cordiformis (Karsten 11°)
two embryo-sacs often oceur; in Delphinium (Mottier 2) two
completed embryo-sacs have been found (Fig. 34), and in Ra-
nunculus (Coulter *!) several sacs develop to the two or four-
nucleate stage (Fig. 25); among the Rosaceae, several embryo-
sacs have been observed to start in Rosa (Strasburger*), Erio-
botrya (Guignard!*), and Alehemilla (Murbeck ®4); and the
same is true of Astilbe (Webb1!1). Among the Compositae,
Marshall-Ward * observed three sacs enlarging side by side in
Pyrethrum, and Mottier °° reports two completed sacs in
Senecio.

The history of the gametophyte from the megaspore to the
completion of the egg-apparatus is remarkably uniform. Atten-
tion has been focused upon it for
many years, and almost every
description is a reiteration of
the preceding one. The mega-
spore and its nucleus usually en-
large very much before divisicn,
and the daughter nuclei migrate,
one to each end of the sae (Figs.
The subsequent divi-
sions proceed rapidly and simul-

35-37).

taneously, resulting in a group
of four nuclei at each end of the :

; Fic. 34.—Delphinium tricorne. Two ma-
embryo-sac. The antipodal po- jure builirsa-tane Ivins cidety sides
lar nueleus and the micropylar one ovule; ).—After Morrie.
polar nucleus (sister to the ege)
then move toward one another and fuse in the general central re-
gion of the sac, forming the primary endosperm nucleus.* The
three remaining micropylar nuclei enter into the formation of
the cells of the egg-apparatus, while the three remaining antipo-
dal nuclei enter into the formation of the antipodal cells. Such

* A discussion of the participation of one of the male cells in the forma-
tion of this nucleus will be found in Chapter VII.

y
‘

8 MORPHOLOGY OF ANGIOSPERMS

(oa)

is in brief outline a history whose beginnings are entirely con-
jectural. Its uniformity throughout so vast a group of plants
testifies to its long establishment. The evanescent cell-plate
frequently observed during the three free nuclear divisions by

Fie. 37.—A, Lilium philadelphicum, second nuclear division in the embryo-sac; the
persistence of the spindle from the first division indicates that the second division
has followed very rapidly; x 450; after Scnarrner.® 5, L. philadelphicum,
third nuclear division; two of the spindles show the beginning of a cell-plate;
x 450; after Coutter.48 C, Ranunculus multifidus, fusion of polar nuclei to form
endosperm nucleus; x 600; after CouLTER®!; s, synergids; 0, oosphere, fusing
polar nuclei in central region: a, antipodals.

which the eight-nucleate stage of the embryo-sac is reached, the
frequent organization of cells about the three antipodal nuclei,
the frequent division of the antipodal cells resulting in a more
or less extensive tissue, and the additional nuclear divisions ob-
served in Peperomia and other forms, are evidenees that the
present female gametophyte of Angiosperms is a much reduced
descendant from multicellular ancestral forms, with forms like
(netum as the nearest approach to the present conditions; but
there seem to be no nearer records of its connection with the
histories of other female gametophytes. The female gameto-
phyte of Angiosperms, therefore, is a morphological problem of

Fie. 35.—Lilium philadelphicum. A, archesporial cell which is also the megaspore
mother-cell; By synapsis: C, stage just before splitting of spirem; J, longitudinal
splitting of spirem (best seen in threads at the left); x 466.—Negatives by W. J.
G. Lanp.

‘
A
2 a’

Fie, 36.—Lilium philadelphicum. £, mitotic figure of the reduction division showing

FY binucleate embryo-

the short, thiek chromosomes characteristic of this stag
suey G, four-nucleate embryo-sac ; //, double fertilization ?: in the egg the darker
nucleus is the male and the lighter one the female: just beyond the ege three

nuclei are fusing; the antipodal polar nucleus forms about one-half of the conplex.
while the micropylar polar nuclens and the mate nucleus form the other half, the
nile nueleus being on the right and touching both polar nuclei, 2£-G x 466;
Hf x 520,—Negatives by W. J. G. Lanp,

THE FEMALE GAMETOPHYTE 89

great obscurity, and very little has been added to the original
suggestions concerning it.

The most important departure from the ordinary history
is that shown by Peperomia pellucida, as described by Camp-
bell 7 and Johnson * (Fig. 38), Gunnera (Schnegg °°), Tril-
lium (Ernst '"*), and Tulipa as described by Guignard.8°* In
Peperomia the nuclei of the embryo-sae do not show any of the
polarity that is so marked a feature in other forms. The first
four nuclei are large, and arranged peripherally like the spores
of a tetrad. Divisions continue until sixteen parietal nuclei,
rather evenly distributed, are found in the sac. One of the
nuclei at the micropylar end of the sac becomes somewhat larger
and is surrounded by a fairly defined mass of cytoplasm with a
limiting membrane, this cell functioning as the egg. Another
micropylar cell is similarly organized, and from its position

Fie. 38.—Peperomiu pellucida, A, longitudinal section of an ovule with a four-nucleate
embryo-sac showing no polarity ; x 295. 6, embryo-sac at time of fertilization ; ¢,
pollen-tube; 0, oospore; e, group of nuclei fusing to form endosperm nucleus; p,
peripheral nucleus of embryo-sac; s, synergid; 2, vacuole; x 520. C, D, groups of
nuclei fusing to form endosperm nucleus; x 520,—After Jounson.7®

may be called a synergid. Eight of the remaining nuclei mass
together, are surrounded by a common cytoplasmic investment,
and after fertilization unite to form a great fusion-nucleus that
functions as the primary endosperm nucleus. The remaining
six nuclei remain in their parietal position and are finally cut

90 MORPHOLOGY OF ANGIOSPERMS

off by walls, showing no tendency to migrate toward the posi-
tion of antipodal cells. This remarkable history is regarded by
Campbell as repre-
senting a primitive
phase of the embryo-
sac of Angiosperms ;
a view from which
Johnson dissents, and
in a more recent pa-
per 14 he shows that
in the allied Piper
and TIleckeria the
eight-nucleate stage
of the embryo-sac is
reached in the usual
way. It is tempting
to connect such a sac

Fie. 39.—Gunnera. A, embryo-sac with nine nuclei,
showing no polarity. ZB, later stage showing sixteen :
nuclei; s, synergid nuclei; 0, oosphere nucleus; near as that of Peperomia

center, a group of six nuclei fusing to form endosperm with such as that of
nucleus; near base, seven antipodal nuclei.—After =
ScHNEGG.103 (rnetum, and theo-

retically it repre-
sents what one might expect to be an earlier condition of
the female gametophyte among Angiosperms; but Johnson in-
fers from the testimony of Piper and Heckeria, just referred
to, that this particular sae of Peperomia is specialized rather
than primitive.

In Gunnera, according to Schnege,!®* there is no polarity
in the early stages of the embryo-sac, and the nuclear divisions
are not simultaneous but irregular, so that there is no definite
eight-nucleate stage of the sac. Before fertilization there are
“at least ” eight nuclei, and very commonly one or more of the
nuclei divide so that nine or ten and sometimes even sixteen
nuclei are found (Fig. 89); in which ease, as in Peperomia,
the primary endosperm nucleus is formed by the fusion of a
considerable number of nuclei. A similar lack of polarity has
been observed in Tulipa sylvestris by Guignard,’?" and in Tril-
lium grandiflorum by Ernst !!°; in the latter ease at least two
of the nuclei of the eight-nucleate sac have been known to di-
vide, giving rise to a sae with ten nnelei.

In the embryo-sae of Juglans regia Nawaschin *§ has indi-

c

THE FEMALE GAMETOPHYTE 91

cated a lack of the usual definite organization, the male cells
being described as “wandering” in the cytoplasm of the sac
and fusing with one of several free nuclei which function as
eges but have not organized into an egeg-apparatus. This loose-
ness of organization in the cells of the embryo-sac has also been
observed by Karsten 1° in several species of Juglans, and he
emphasizes the resemblance to Gymnosperms, believing that
Angiosperms are derived from them, with such forms as
Gnetum as the point of origin,

What may be called minor irregularities in the structure of
the female gametophyte have been described in a number of
forms. The reported occurrence of only one synergid in Orni-

Fie. 40.—Helosis guyanensis. A, binucleate embryo-sac with antipodal nucleus already
disintegrating. &, later stage; micropylar nucleus has divided twice, giving rise to
two synergids, an egg (not shown), and the micropylar polar nucleus which gives
rise to the endosperm; no antipodals. C, remains of synergids and egg; the
“pseudo-endosperm” nucleus dividing; no trace of antipodals.—After Cuopar and
BERNARD.®3

thogalum nutans, Santalum, Gomphrena, and Loranthus, has
long been known. In Loranthus Treub }* says that this is due
to the fact that the primary micropylar nucleus divides only
once, but it is also possible that the mother-nucleus of the

92 MORPHOLOGY OF ANGIOSPERMS

synergids may not always divide. In the same category Casu-
arina, as reported by Treub,?° has long been included; but a
recent study of the genus by Frye 1!® las shown that the usual
three micropylar nuclei occur. Fischer ©
reports the occurrence of two eges in
Gomphrena, which Strasburger suggests
may have come from division of the nor-
mal ege.

In Loranthus and Casuarina Treub
also states that there are no antipodals ;
but Frye’s 1!" recent investigation of the
latter form has resulted in the discovery
of three antipodals, which occur either
at the chalazal extremity of the expand-
ed portion of the sac, or in the tubular
haustorial elongation.

In /Telosis quayanensis (Balanopho-
raceae) Chodat and Bernard ** state that
the primary antipodal nucleus (binu-
cleate stage) rarely divides, but soon de-
generates, which means also the absence
of an antipodal polar nucleus (Fig. 40).
The same phenomenon has been ob-
served by Hall ?°° in Limnocharis, the
primary antipodal nucleus remaining
undivided. Several eases have also been
reported in which regularly formed po-
lar nuclei approach one another but do
not fuse before endosperm formation, as
in Balanophora elongata (Treub **),
confirmed also in B, indica by Van Tie-
45

Fia. 41.— Antennaria alpina.
Egg-cell much extended -
and polar nuclei about to gnem,
divide; a, antipodal cells; but in the allied Rhopaloenemis (Lot-
¢ egg; P, polar nuclei; s, 2. 82) the polar nuclei fuse. In the or-
synergid; m, micropy le ; ines . ‘ is =
x 250.—After Juwy.74 celid Gymnadenia also, Marshall-Ward 7

states that the polar nuelei do not fuse;
in the parthenogenetie Antennaria alpina Juel 57 (Fig. 41) ob-
served the same phenomenon ; in Lemna Caldwell °? reports that
the polar nuclei often do not fuse; and in Juglans nigra Kar-
sten '!® states that there is probably no fusion of polar nuclei, or

and in B. globosa by Lotsy °°;

;

THE FEMALE GAMETOPHYTE 93

if it takes place at all it is very late. In parthenogenetic species
of Alchemilla (Murbeck 11°), not only the two polar nuclei have
the power of motion, but the synergid and antipodal nuclei may
also move toward the center of the sac, forming groups of three,
four, or five “ polar nuclei” surrounded by a common mass of
protoplasm. In the case represented in Fig. 42, Murbeck inter-
prets the antipodals to be lacking, although, according to his
own account, their nuclei are in the group
of what he calls “ polar nuclei.”

Notwithstanding some such irregulari-
ties, however, the normal history of the
female gametophyte is so remarkably con-
stant that none of them can be regarded
as of special significance.

The cells of the egg-apparatus are alike
in being pyriform and bounded by a mem-
brane which, for the lack of an accepted
English equivalent, is commonly desig-
nated the Hautschicht; the egg, however,
is vacuolate toward the micropyle, its nu-
cleus lying at its broad extremity, while in
the synergids the reverse is true (Fig. 43).
The size of these cells, as compared with
the other cells of the embryo-sac, is ex-
eeedingly variable, sometimes being much
the largest and sometimes even the small-
est. The morphological nature of this
group of cells has been much discussed in Fis. 42.—Alehemilla serv-

‘ . cata, ‘“ Embryo-sac with
the attempt to relate it to the archegonium donipliete-ede-appscutns
of the lower plants. There seems to be no and five polar nuclei; in
serious objection to regarding all three — @greement with this, no

‘ . . antipodals are present.”
cells as potential eggs, only one of which = _ afer Murnpex.t
usually functions as such. Whether they
represent three archegonia, or the egg and canal cells of one
archegonium, seems to be pressing morphology to an absurdity.
The lack of any compact tissue precludes the formation of an
archegonium, and hence free cells organize as eggs. There
seems to be no need to relate them to archegonia, but merely
to regard them as eggs produced by a gametophyte that can not
form archegonia. If a rigid morphology is to be applied, it

94 MORPHOLOGY OF ANGIOSPERMS

may be said that these eggs appear earlier in the history of the
gametophyte than is possible for archegonia, which are rela-
tively late structures.

The character and behavior of the egg will be discussed
under fertilization, but the synergids present certain peculiari-
ties that may be considered here. The name “ synergid,” given
by Strasburger, has proved most ap-
propriate, for it is usually both a nu-
tritive and mechanical “ helper” in
the process of fertilization, although
it does not “serve to convey the fer-
tilizing substance from the pollen-
tube to the oosphere,” as once sup-
posed. The two synergids follow the
configuration of the apex of the sac,
which is usually rounded, and hence
Fie. 43.— Lblygonum divarica- they are pyriform for the most part.

tum. Embryo-sac ready for , Ser

fertilization: showing syner- Ln certain cases, however, the sac be-

gids with “filiform appara~ comes pointed or even much elon-

eens es gated, and the synergids develop

STRASBURGER.S beak-like extensions of more or less
prominence, which in many cases

have been found to pierce the wall of the embryo-sac and
extend into the micropyle (Fig. 44). Occasionally the beaks
show delicate longitudinal striations, and were called by Schacht
the “filiform apparatus.” Such beak-lke extensions of the
sac and synergids are usually associated with narrow and long
micropyles, and doubtless are of assistance in the progress of
the pollen-tube. Among the Monocotyledons they are by no
means so Common as among Dicotyledons, but are well scat-
tered among the families. For example, they oceur in Sorghum
and Zea (Guignard ™), Hichhornia (Smith **), Crocus (Hot-
ineister 1), Romulea (Ferraris !*°), and Gymnadenia (Marshall-
Ward 7), and doubtless in others. Among the Archichlamydese
they are more numerous, having been noted in Salix (Chamber-
lain #8), Quercus (Conrad 8), Santalum, Polygonum (Strasbur-
ger), Hepatica (Mottier °°), Thalictrum (Overton 1°), Silene
and Capsella (Guignard '*), and becoming very long in Euphor-
bia (Miss Lyon **) and Siwm. They are even more common
among the Sympetalae, a fact perhaps to be associated with the

THE FEMALE GAMETOPHYTE 95

very heavy integument. They have been noted, for example, in
Campanula, Jasminum, and Salvia (Guignard !*), and in almost
all the species of Compositae investigated. In Calendula lusi-
tanica Billings !°° reports a very conspicuous synergid hausto-
rium, the synergids developing into the micropyle and much
enlarging. Synergid haustoria have been reported in other
forms, which are probably outgrowths of the sac. The behavior
of the synergids of Trapella, as described by Oliver,?! is re-
markable, after fertilization increasing much in size, and in
the mature seed forming a conspicuous tubercle-like body
(Fig. 32).

It has been generally assumed that the polar nuclei fuse as
soon as formed, which is perhaps generally true. If the time
of fusion be related to the act of fertilization, however, it will
be found to vary from before pollination to long after fertiliza-
tion, and in some cases, already mentioned (Lemna, Gymnade-
nia, Balanophora, Antennaria alpina), the polar nuclei seldom if

Fie. 44.— A, Salix petiolaris, upper end of embryo-sac soon after fertilization : p, pollen-
tube: s, synergid: the synergids, which are beaked and have the “ filiform appara-
tus,” have broken through the embryo-sac into the micropyle; x 694. BS. glau-
cophylla, synergids not disintegrating after the formation of the embryo; polar
nuclei have not fused; x 694.—After CHAMBERLAIN."

ever fuse. In this connection it may be noted that there is no
antipodal polar nucleus in Limnocharis (Hall?) and Helosis
(Chodat and Bernard §*). Fusion of the polar nuelei at any
time from before pollination, as in Hichhornia (Smith °*), to
the moment of sexual fusion, as in Liliwm, may be regarded as
normal. Later fusion of the nuclei has been noted in the

96 MORPHOLOGY OF ANGIOSPERMS

Nyetaginaceae and Conyza by Guignard,’? in Alchemilla by
Murbeck,’4 in Sium, in which case they are relatively small and
remain near one another in a parietal position until the em-
bryo-sac has become much enlarged, in Nicotiana by Guig-
nard,!’? and in Juglans nigra by Karsten,’? in which there
may be no fusion. In this connection the recent experiments
of Shibata !?? upon Monotropa uniflora are of interest. He
found that the polar nuclei may fuse in the absence of pollina-
tion, but that fusion is hastened by pollination. For example,
when pollination oceurs the polar nuclei fuse in about five days,
lmt when pollination is prevented the fusion does not occur for
ten days or more,

It seems to be generally true that the polar nuclei either
fuse in contact with the egg, as observed by Guignard 1?” in
Eriobotrya, Cuphea, Nicotiana? and other forms, or the
fusion-nucleus migrates to that position just before fertiliza-
tion, as in Tricyrtis (Ikeda 1°"), or after fertilization, as re-
ported by Balicka-Iwanowska °* for the Scrophulariaceae and
allied families. The last observer suggests that this position of
the primary endosperm nucleus has to do with the nutrition of
the fertilized egg; but the case of Tricyrtis suggests a function
during fertilization. It is certainly true that in most cases
this nucleus is finally either in contact with the egg or very
near to it. In Sagittaria (Schaffner 47) and Potamogeton
(Holferty °7) the polar nuclei fuse in the antipodal end of the
sac, but at the first division of the fusion-nucleus one daughter-
nucleus moves toward the egg-apparatus. The evidence seems
to show that the polar nuclei and the fusion-nucleus have
freedom to “ wander ” through the sac, and that there is at some
time a relation in position to the ege. For example, in T'ri-
cyrtis Ikeda 1° has deseribed the fusion-nucleus as passing first
to the antipodals, and then passing to the egg just before fer-
tilization.

The antipodal cells are either naked or invested by walls,
and are exceedingly variable as to their arrangement, number,
and persistence. The ordinary statement that the number of
cells is limited to the three primary ones, and that they are more
or less ephemeral, taking no part in the activities of the embryo-
sac, has proved to be far from true in the majority of cases
investigated. It is impossible to classify them as ephemeral

THE FEMALE GAMETOPHYTE 97

and inactive, or relatively persistent and active, for the grada-
tions between these two extreme conditions are complete. It
is noticeable, however, that the two conditions are apt to be
characteristic of families, and that the most extensive develop-
ment of the antipodal cells is found in comparatively few
families.

It is needless to attempt to give a complete list of those
families in which the antipodal cells are ephemeral, disorgan-
izing with more or less rapidity, and apparently taking no part
in the activities of the embryo-sac. The following data will
serve to illustrate that this condition is found in groups of
every rank. Among Monocotyledons, ephemeral antipodals
are found in Typhaceae, Naiadaceae (Potamogeton), Alisma-
ceae, Pontederiaceae, Liliaceae (except Ornithogalum), Sei-
tamineae, and Orchidaceae; among Archichlamydeae, in Sau-
ruraceae, Salicaceae, probably Casuarinaceae, Cupuliferae,
Loranthaceae (Loranthus), Caryophyllaceae, Cruciferae, Saxi-
fragaceae, Leguminosae, Euphorbiaceae, Aceraceae, Cactaceae,
Onagraceae, and Umbelliferae; and among the Sympetalae, in
Oleaceae, Bignoniaceae, Pedaliaceae, Scrophulariaceae and
their allies, and certain Rubiaceae. <A certain amount of varia-
tion in these families has been found, as will be noted later,
and doubtless much more will be found as other species are
investigated. It will also be noted that this condition is
probably not so prevalent in the Sympetalae as in the other
groups.

In those antipodal cells that function more or less there is
every degree of prominence. It should also be noted that antip-
odals of the same sac often differ very much in prominence. For
example, in Lilium the innermost antipodal is often the most
prominent, in Nicotiana (Guignard 1°") they are often unequal
in size, among the Galieae (Lloyd °°) one of the three is much
elongated, and among the Compositae the one nearest the cha-
laza is often very much enlarged (Fig. 47). The simplest cases
are those in which the cells do not grow very large or divide,
but by their prominence and persistence indicate that they are
taking some part in the activities of the embryo-sac, as in
Viscum, Nyctaginaceae, Ruta, Polygala, Borago, Salvia, Nico-
tiana, and Sarcodes, as well as certain members of families
characterized by a striking development of the antipodal cells.

98 MORPHOLOGY OF ANGIOSPERMS

In other instances the activity of the antipodal cells is
shown by their great increase in size and usually multinucleate
condition, and also by their more or less extensive division.
Among the Monocotyledons, the Sparganiaceae, Gramineae,
and Araceae are conspicuous for their strongly developed antip-
odal cells. In Sparganium simplex Campbell ®* describes the

Fic. 45.—Sparganium simpler. Lower end of embryo-sac showing a large mass of
antipodal cells. —After CAMPBELL.°9

antipodal cells as at first very small, but immediately after
fertilization they enlarge to several times their original size,
their nuclei dividing. Finally, a conspicuous hemispherical
mass of 100 to 150 uninucleate cells is formed, at this stage the
endosperm having hardly at all developed (Fig. 45). The
strong development of antipodal cells among the Gramineae
has long been known, Fischer ® having reported in 1880 that
each antipodal cell of Lhrarta panicea divides once, and of
Alopecurus pratensis three or more times. More recently
Cannon * found in Avena fatua that the antipodal cells be-
come thirty-six or more in number before fertilization, and
begin to disorganize with the beginning of endosperm devel-
opment. Westermaier ** has described a growth of antipodal
tissue in Zea and other grasses before fertilization, and
Guignard *° has found as many as twelve multinueleate cells
in the much narrowed antipodal end of the embryo-sae of
Zea. It is of interest to note in this connection that in 1882
the same investigator ?* found in Cornucopiae undivided but
prominent and often binucleate antipodal cells. Among the
Araceae Campbell ™ states that there is a general tendency for
the antipodals to develop strongly, often dividing and forming
a tissue, and in Lysichiton hamlschatcense the same observer °*
finds that at the time of fertilization the antipodal nuclei have

THE FEMALE GAMETOPHYTE 99

increased remarkably in size, and after fertilization the cells
increase rapidly and divide, forming a group of eight or more
cells with remarkably large nuclei. In addition to these three
monocotyledonous families, a prominent antipodal region has
been found in Triglochin maritima (Hill*®), in which there
are three to fourteen cells; very large but undivided antipodals
have been found in Lilaea (Campbell °°), Commelina (Guig-
nard !*), Ornithogalum, Gladiolus, and Crocus (Mottier *°),
Narcissus and [ris (Guignard 1?), and Romulea (Ferraris 1°") ;
and Ikeda 1°° reports that in T'ricyrtis the antipodals fill up
the “ chalazal protuberance,” become elongated with it, and
reach their maximum length just before fertilization.

Among the Archichlamydeae, the Ranunculaceae are espe-
cially characterized by the activity of the antipodal cells, shown
both by their great size and
multinucleate condition, and
also by their divisions. We
have records of twelve genera,
and in all of them the antipo-
dals are conspicuous. In 1879
Strasburger ® reported the an-
tipodals of IMyosurus as very
prominent, and in 1882 Guig-
nard 17 deseribed the antipodals
of Hrianthis as large, those of
Clematis as very large and bi-
nucleate, and those of Hepatica
as forming a great group and
becoming multinucleate after
fertilization. In 1890 Wester-

23

maier

reported large antipo-
dals in Ranunculaceae, among

4 . 1 ry ‘ :
them J igella ; and in 1895 Fie. 46.— Aconitum Napellus. Longitudi-

Mottier ?° investigated a num- nal section of embryo-sac after fertili-
, : . vation, showing the three very large
ber of genere and deseribed the zation, showing the three very large

— . antipodals: nuclei of endosperm in mi-
antipodals of Delphiniwm tri- fdiee 4 th abies semen arent

corne as very large, growing

with the embryo-sac, and persisting till after fertilization;
those of Caltha palustris as large, pyriform, and multinu-
cleate; those of Aquilegia canadensis as growing enormously

100

MORPHOLOGY OF ANGIOSPERMS

before and after fertilization and becoming multinucieate ;
those of various species of Ranunculus, Anemonella, and Thal-

ictrum dioicum as very large; and
those of Hepatica as growing very
much until after fertilization. Since
then Overton 1! has found that the
antipodals of Thalictrum purpuras-
cens become remarkably large, reach-
ing the center of the sac; Miss
Dunn *® has reported that in Del-
phinium exaltatum three very large
antipodals persist even in the oldest
seeds with no indication of degen-
eration; Miss Lyon has noted as
many as twenty-five antipodal cells
in Hepatica; and Osterwalder °° has
figured exceedingly large antipodals
in Aconitum Napellus (Fig. 46).
The whole family is characterized,
therefore, by the activity of its an-
tipodal ceils, exhibited more by their
great increase in size than by divi-
sion. Among the Amentiferae Miss
Benson *4 reports a row of six or
more superposed antipodals in the
very narrow antipodal end of the
sac in Castanea vulgaris, the lowest
one being figured as the largest and
multinucleate, the whole structure
resembling the antipodal region of
many Compositae. Around the base
of this elongated antipodal region
there are developed such tracheid-
hke cells as oceur in the nucellus

Fie. 47.— Aster novae-angliae. Longitudinal sec-
tion of embryo-sac just before fertilization ;
m, micropyle; s, synergid ; 0, oosphere; e, en-
dosperm nucleus; ¢, jacket; 2, lower antipodal
cell; four other antipodal cells shown, the
upper with four nuclei and the others with two;
x 407.—After CHAMBERLAIN. $5

THE FEMALE GAMETOPHYTE 101

of Casuarina, but in this latter
instance they are derived from
mother-cells. Other Archichlam-
ydeue with active antipodals are
ITeckeria (Johnson 434), in which
they are sometimes six to eight in
number; Asarum (Hotmeister 7),
in which they are very long, ex-
tending at fertilization from one-
third to one-half the length of the
embryo-sac, and sometimes divi-
ding; Jeffersonia diphylla (An-
drews 7), in which they become
about one-half as long as the
embryo-sac; Hriobotrya (Guig-
nard ?*), in which they are large ;
and Anoda (Guignard?*), in
which they are prominent and
often binucleate.

Among the Sympetalae the
Compositae are especially note-
worthy for the extensive develop-
ment of the antipodal region ( Fig.
47). In this family the chalazal
end of the elongated sac is very
narrow and the antipodals are
superposed. In a number of
cases, as in Doronicum, Petasites,
and Taraxacum, there are usually
only three antipodals, but they
remain active; while in Tussila-
go (Guignard 1”) there are usual-
ly four; in Senecio (Mottier **)
two to six; in Silphium (Mer-
rell 77) three to eight; in Conyza
(Guignard!*) eight to ten; in
Aster novae-angliae (Chamber-
lain *°) three to thirteen ; and in
Antennaria (Juel*®7) they con-
tinue to divide until quite a tis-

Fic. 48.—A, Sherardia arvensis. Em-
bryo-sac before fertilization ; low-
er antipodal acting as an hausto-
rium. BL, Callipeltis ecucullaria,
showing lower antipodal still act-
ive after embryo and endosperm
are considerably advanced.—A fter
Lioyp.1%

102 MORPHOLOGY OF ANGIOSPERMS

sue is formed (Fig. 41). This record indicates that the divisions
are variable in number even in the same species, and it may
be noted in this connection that while Schwere ** states that
there are only three antipodals in Taraxacum, Hegelmaier ?
had previously reported four or five, and more than three have
been observed frequently in this laboratory. In many of these
cases all the cells usually contain two or more nuclei, and the
end cell toward the chalaza often becomes vesicular and multi-
nucleate, breaking through the sac and encroaching upon the
chalazal tissue. It seems to be clear that in the Compositae
this development of antipodals is practically an aggressive haus-
torium for the embryo-sac; while in the Ranunculaceae the
antipodals doubtless serve as an haustorium, but do not invade
the neighboring tissue. Certain Rubiaceae also contain active
antipodals, since Lloyd ®* has found that in Vaillantia hispida
while two of the antipodals are insignificant, the third is very
prominent and remains active for a long time. The same au-
thor 1°° has more recently found the same to be true of the
Galieae (Fig. 48), and he also has found four to ten antip-
odals in Diodia virginiana. Balicka-Iwanowska ® has also
noted enlarging and persistent antipodals in Plantaginaceae and
Campannlaceae, and their division in Dipsaceae as in the Com-
positae. In Asclepias, although three active antipodals are
usual, Frye 1** has observed compact antipodal tissue consisting
of seven or eight cells; and in A. Cornuti he has noted the
occurrence of tracheid-like cells at the base of the embryo-saec,
such as occur in Casuarina and Castanea.

There seems to be no reason to question the ordinary view
that the antipodal cells are vegetative cells of the gametophyte.
Their polarity as contrasted with that of the ege-apparatus,
and their behavior when they function confirm it. The ocea-
sion for their activity seems to he to supply the embryo-sae with
nutritive material absorbed from without at a time when the
endosperm has not been organized or other means of obtain-
ing nutrition are not available. Tn Monotropa uniflora Shi-
bata 1** has found that the three small antipodals disintegrate
after fertilization, but that when fertilization is prevented they
may enlarge enormously and fill a considerable portion of the
sac. The character of the active antipodals among the more
primitive Monocotyledons and in the Ranunculaceae may be

THE FEMALE GAMETOPHYTE 103

regarded as indicating a primitive condition of the nutritive
tissue in the female gametophytes of Angiosperms; but the
antipodals of many of the Compositae are organized into an
aggressive haustorium which can only be regarded as a very
specialized organ.

The enlargement of the embryo-sac and the nature of its
development, both before and after fertilization, are extremely
ee The enlargement is directly related to the digestion
of the contiguous tissue. In a few cases this destruction is not
extensive, and more or less of the nucellar tissue is permanent
(perisperm) and is used for the storage of reserve food, as in
the Scitamineae, Piperaceae, Chenopodiaceae, Phytolaccaceae,
Caryophyllaceae, Nymphaeaceae, ete. In most cases, however,
the destruction of the nucellar tissue is complete to the integu-

ment, and even that is sometimes ae as in Allium odo-
rum, certain orchids, and Astilbe (Web Bay, Frequently the
tissue at the apex of the nucellus remains as a cap on the em-
bryo-sac, as in Arisaema (Mottier?7) and other Araceae,
Lemna (Caldwell ®*), Liliaceae, Silphiwm (Merrell), and
many other forms, and this is frequently accompanied by more
or less elongation and even division of the capping cells.

Frequently a definite nutritive jacket invests the embryo-
sac, consisting of one or more layers of cells with deeply stain-
ing contents (Figs. 47, 50). For the most part this is a single
layer derived from the integument, but in Armeria it is derived
from the nucellus, and in Hrodium one layer is derived from
the nucellus and the other from the integument. This jacket
has been called a tapetum, and such it is in function. In using
the term, however, there is danger of confusing it with the
tapetum of ordinary sporogenous tissue. This jacket has been
definitely observed as conspicuous in ffelosis (Chodat and
Bernard **), Siwm, many Serophulariaceae (Balicka-Iwanow-
ska %), Campanula (Barnes '*), Stylidaceae (Burns *’), and
certain Compositae, and by Billings 19° in numerous sympeta-
lous forms, among the most conspicuous being Lobelia, Primu-
laceae (except Leptosiphon), Linum, Bonsiihice Arsene
Menyanthes, Polemoniaceae, Myoporum, Globularia, Scaevola,
Calendula, ete.

In many eases the micropylar end of the sae destroys all
of the nucellar tissue capping it, and protrudes more or less

8

104 MORPHOLOGY OF ANGIOSPERMS

into the micropyle, as in Hemerocallis, Crocus, Gladiolus,
Romulea (Ferraris 12°), Alchemilla (Mnurbeck **), in which the
sac pushes through to the tegumentary tissue closing the micro-
pyle, Medicago, Torenia asiatica (Strasburger *), Labiatae,
Vaillantia (Lloyd °), Diodia and the Galieae (Lloyd?°°), and
many other forms. In Vaillantia the mother-cell migrates into
the micropyle and develops there.

While ordinarily the embryo-sac is relatively broad and
rounded at its micropylar extremity, this is by no means so
commonly true of the antipodal
end. If the antipodals are ephem-
eral, the growth of the antipodal
region is frequently checked after
the first division of the megaspore
nucleus, and through the growth of
the rest of the sae it becomes a
very small pocket, as in Typha,
Potamogeton, Sagittaria, certain
Gramineae, Pontederia, Lilium,
Oenothera, ete. (Fig. 79). It is
generally true that the antipodal
region of the sac is narrower than
the micropylar, but its growth is
not often checked so completely
and so early as in the cases cited.

In other cases, the antipodal

region of the sac grows very active-
Fie. 49.—Saururus cernuus. Longi- iy elongating toward the chalazal
tudinal section of embryo-sac; region and penetrating it more or
after the first division of the en- ;
dosperm nucleus the mieropylar =
gelll has given rise 10 endosperm TOW and elongated sac. Such an

tissue, while the other cell has antipodal region must be regarded
become a large vesicular hausto-

less deeply, resulting in a very nar-

as an haustorium that digests and
absorbs its way into the chalazal tis-
sue. Illustrations of this are very numerous, as in Gramineae,
Tricyrlis (Ikeda 1°"), Seitamineae, Saurnraceae, Loranthaceae,
Polygalaceae, Lythraceae, Aceraceae, and most Sympetalae.
In penetrating the chalaza the antipodal tip usually remains
narrow, but in Sauruwrus (Johnson 87), Seitamineae (Tim-
phrey *°), Cuphea (Guignard 1"), Campanula (Barnes 38), ete.,

rium.—A fter Jounson.87

THE FEMALE GAMETOPHYTE 105

it has been observed to enlarge more or less abruptly, forming
a bulbous chalazal haustorium. In Canna indica this becomes
much larger than the rest of the embryo-sac; and in Saurwrus
cernuus Johnson ** describes the embryo-sae as elongating rap-
idly, broadening below, the upper part remaining narrow, the
completed sac resembling a long-necked flask (Fig. 49).

In addition to the various forms of haustorial apparatus
described above as developed in connection with the embryo-sac,
certain extreme cases deserve special mention. It has long
been known that among the Santalaceae (Santalum, Thesium,
Osyris, ete.) the embryo-sac develops a micropylar tube that
passes through the micropyle and enters the cavity of the ovary,
and that in some of then: (Vhesium, ete.) there is also an antip-
odal tube (see Guignard!7). These remarkable tubular or
vermiform haustoria obtain nutritive material beyond the ovule.
Later, Johnson ** described in detail the haustorial apparatus
ot Myzodendron, another genus of Santalaceae. The young sac
is broad above and narrowed toward the antipodal end. After
fertilization the antipodal region develops rapidly, penetrates
the chalaza, enters the placental axis, and curving passes down
it to the base of the flower, where its tip dilates and becomes
embedded in the * vascular cup” formed by the three diverging
carpellary bundles. Rigidity is given to this remarkably elon-
gated tube by numerous cross-walls, but these are lacking in the
placental region.

Among the Amentiferae (Miss Benson *!) vermiform caeca
are often sent out from the embryo-sac. In Fagus sylvatica
this tubular outgrowth penetrates to the base of the nucellus,
the primary endosperm nucleus passing into it, but not the
antipodals, which are anchored by thick walls. In Castanea
vulgaris the caecum develops from the side of the sac just above
the narrow antipodal prolongation, is entered by the endosperm
nucleus, and passes down between the nucellus and the integu-
ment. In Carpinus Betulus the chalazal region is sometimes
riddled by the long caeca from the several embryo-sacs; and in
Corylus Avellana a short caecum appears after fertilization.

In Casuarina, as shown by Frye,?® a conspicuous vermi-
form caecum is developed much as among the Amentiferae.
From the antipodal extremity of the sac a long tube penetrates
the chalazal region, into which the endosperm nucleus passes

106 MORPHOLOGY OF ANGIOSPERMS

and sometimes the antipodals. This haustorial tube was ob-
served to begin its development at different stages in the history
of the sac, sometimes being evident in the two- nucleate stage
of the sac, sometimes not having begun in the seven or eight-
nucleate stage.

One of the strangest cases is that of T'rapella, as described
by Oliver.2!. In this the innermost megaspore of a row of four
becomes extremely elongated, penetrates the chalaza, and
divides longitudinally, the two cells being very active, as indi-
cated by their contents and numerous starch grains. In this
form the synergids enlarge and persist on the apex of the sae
(Fig. 32).

Among the Scrophulariaceae, such as Pedicularis, Rhinan-
thus and its allies, etc., Tulasne, Hofmeister, Tschirch, Schlot-
terbeck, and others have described the numerous vermiform
tubes that develop from the embryo-sac and ‘ ruminate”’ the
integument and destroy its tissue, although they did not recog-
nize.their origin; and similar tubes have been found in certain
Labiatae. Recently Balicka-Iwanowska °* has investigated the
embryo-sacs of many Serophulariaceae, as well as other allied
Sympetalae, and has discovered a remarkably constant occur-
rence of haustorial outgrowths from the sac at both micropylar
and chalazal ends, filled in later by endosperm cells. The
common case is for the broad micropylar end of the sac to de-
velop four prongs, and for the narrower chalazal end to fork,
as seen not merely among Scrophulariaceae, but also among
Utriculariaceae, Pedaliaceae, and Plantaginaceae. The devel-
opment of these haustoria is related to the thickness of the
integument, which in these groups seems to be a source of nutri-
tive supply. There are all stages in the development of the
haustoria, but the general tendency i in this region of the Sympet-
alae is very marked. <A striking case is that of the well-known
Torenia asiatica, mentioned above, in which the sae does not
develop outgrowths, but protrudes bodily beyond the micropyle,
touching the funiculus, and even reaching the ovary wall. All
of these haustorial outgrowths are supplied with active endo-
sperm cells or nuclei.

It is stated that all species of Campanulaceae (Balicka-
Twanowska ®), Lobeliaceae (Billings!°°), and Stylidaceae
(Burns *°) ae both micropylar and chalazal haustoria, and

AU
\\
ay

sy
ii

Hadith NY)
Halle \ uy

Fie. 50.—A, Globularia cordifolia, the micropylar end of the embryo-sac has grown
out into an extensive haustorium furnished with nuclei from the endosperm; f,
funiculus; after Brrtives.1 2, Plantago lanceolata, longitudinal section of ovule
after embryo is somewhat advanced, showing extensive haustorial system; after
Bariocka-[wanowsKa.*® C, Stylidium squamellosum, embryo-sac after second
division of endosperm nucleus; e, egg; p, pollen-tube; after Burns.86 D, Byblis
gigantea, longitudinal section of seed with branching haustoria in both micropylar
and antipodal regions; 4, haustorium; g, embryo; e, endosperm; after Lana.®}

107

108 MORPHOLOGY OF ANGIOSPERMS

that often finger-like processes are put out at the side or base
of the sac, extending toward the vascular bundles; and in Sty-
lidaceae, immediately after the entrance of the pollen-tube, the
micropylar part of the embryo-sac grows out Into an enormous
haustorium much larger than the rest of the sac (Fig. 50). As
a result of his investigations of Polypompholyw and Byblis,
Lang *! not only discovered conspicuous haustoria, but used this
character, along with others, such as the nucellus with a single
row of axial cells, the tapetum de-
rived from the single integument,
and the united petals, to remove
these genera from the archichlamy-
deous Droseraceae to the sympetalous
Lentibulariaceae.

The whole subject of the mecha-
nism for the nutrition of the embryo-
sac deserves more detailed attention
than it has received. In his study of
the fleshy plants, D’Hubert,** on the
basis of the appearance and disap-
pearance of starch, concludes that the
antipodals nourish the sac before fer-
tilization, the synergids nourish the
nuclei of the pollen-tube and then
the nucleus of the ege at the time
of fertilization, and the polar nuclei
nourish the fertilized ege and give

Fie. 51.—Phyllocactus. Starch dis-
appearing from antipodals and 2 Fs iz
accumulating in other portions TISC to the endosperm ( Fig. 51).

of the embryo-sac; a, antipo- Such details may prove true for the
barman alee Cactaceae and other fleshy plants,*
BERT.33 but the larger field is to be traversed
first, which embraces all of the mor-

phological structures used in obtaining nutritive supplies for
the structures within the embryo-sae, both before and after fer-
tilization. Just what mechanism supplies what strneture is a
subordinate detail and very difficult to prove, besides being an
exceedingly improbable division of labor among structures so

*D'Hubert concludes that starch is characteristic of fleshy plants, but
there is a large display of stareh in Asfi7be (Webb ™) and Galium (Lloyd ™),
and doubtless in many other non-fleshy plants.

THE FEMALE GAMETOPHYTE 109

closely associated. From the data more or less scattered through
the preceding and following pages, the various methods by which
nutritive supplies are brought into the sac may be grouped to-
gether as follows, although the subject is in no condition as yet
for satisfactory organization.

The digestion and absorption of adjacent tissue by the en-
larging sac is the most general method of obtaining nutritive
supphes. It always occurs to a certain extent, and often is the
only observed method. The varying amount of tissue destroyed
in this way is a thing of common observation.

The organization of a definite layer or layers of cells about
the embryo-sac in its later stages, which we have called the
“nutritive jacket,” has not been reported for the Monocotyle-
dons, occurs in comparatively few Archichlamydeae, while it
seems to be common among the Sympetalae. For the origin
and occurrence of this jacket see page 101. Its appearance and
function is that of a tapetum, and there seems to be no good
reason why it should not receive the name.

Tracheid-like cells have been reported in the nucellar tissue
of Casuarina, Castanea, and Asclepias, but this meager list will
doubtless be much increased. That such cells are connected
with a nutritive mechanism seems clear, but their rare and
feeble development suggests a relic of an efficient ancestral
mechanism. The recent discovery (Oliver 1°*) of a Palaeozoic
fern with certain resemblances to the Cycadofilices, in which
tracheids replaced the tapetum in the sporangium, may be an-
other indication of the former somewhat extensive use of this
special form of mechanism. Thick-walled cells often appear
in the chalazal region, especially in connection with the pene-
tration of the sac. Some are as hard as tracheids, while in
other cases the walls have become mucilaginous and swollen.
Similar cells also occur wherever haustoria invade tissue in any
other region of the ovule or outside of it.

The aggressive penetration of the chalazal region by the
elongation of the antipodal extremity of the sac is very common.
This definite antipodal haustorium seems to be nearly always
developed when a more or less prominent mass of chalazal tissue
ocenrs. Among Monocotyledons such haustoria are recorded
among the Gramineae, Liliaceae, and Scitamineae; among the
Archichlamydeae they are known to occur among the Sauru-

110 MORPHOLOGY OF ANGIOSPERMS

raceae, Loranthaceae, Nymphaeaceae, Polygalaceae, Lythra-
ceae, and Aceraceae, while they seem to be almost universal
among the Sympetalae. In most cases the advancing tip re-
mains narrow, but sometimes it becomes enlarged, in certain
eases very much so, For example, in Canna the antipodal
haustorium becomes a bulbous structure larger than the rest
of the sac, while in Suururus the narrow micropylar end and
the bulbous antipodal haustorium form a flask-shaped sac.

Among the Santalaceae the vermiform haustoria sent from
the micropylar extremity of the sac into the cavity of the ovary
have been noted. Perhaps the most remarkable member of the
family in this regard, however, is Myzodendron, as described
above. In this case the haustorium is really an extreme devel-
opment of the antipodal extremity of the sac, but the elonga-
tion is so excessive that it has been included in this rather than
in the preceding category. Among the Fagales vermiform
haustoria are more or less prominent, in this case being sent
out laterally from near the antipodal extremity and penetrating
the chalazal tissue, and being entered by the endosperm nucleus.
Conspicuous haustoria of this type are reported, as noted above,
in Fagus and Castanea, while in Carpinus the chalazal region
is sometimes riddled by the haustoria from the several sacs.
Among the Sympetalae vermiform haustoria are common, being
well known among Serophulariaceae and their allies, as well as
among the Campanulaceae, Lobeliaceae, and Stylidaceae. In
addition to the penetration of the chalazal tissue by haustoria
from the antipodal region of the sac, micropylar haustoria are
often sent into the tissue of the massive integument. Four
such micropylar haustoria, more or Jess prominent, and always
associated with active endosperm cells, seem to be eommon
among the Scrophulariaceae. Such haustoria are apt to be coe-
noeytic, the endosperm consisting of large and densely stain-
ing nuclei rather than of walled cells as in other parts of the
sac. The haustorial mechanism is evident even when it con-
sists only of groups of active endosperm cells in contact with
definite regions of the sae wall.

In this connection the remarkable ease of Trapella (Peda-
laceae) may he mentioned, in which the innermost megaspore
of the linear tetrad becomes modified into an active haustorium
that penetrates the chalazal region (Fig. 32).

THE FEMALE GAMETOPHYTE 111

The protrusion of the sac bodily into or through the micro-
pyle may be regarded as only a more extensive development of
the vermiform micropylar haustorium, but it deserves separate
mention. Y'orenia is the oldest and most conspicuous illustra-
tion of this phenomenon, the sac passing beyond the micropyle
and even reaching the wall of the ovary. The phenomenon
also occurs among the Rubiaceae, the sac entering the micro-
pyle in Diodia and the Galeae, while in Vaillantia the mega-
spore mother-cell passes into the micropyle and divides there.

The projection of the synergid as an haustorium has been
observed by Billings! in Calendula lusitanica, in which the
synergid develops into the micropyle and enlarges greatly ; and
in Trapella (Oliver *1), large, persistent synergids oceur, which
are evidently haustorial. Other synergid haustoria have been
reported, as in Lobelia, but they prove to be merely haustoria
from the sac, containing endosperm.

The antipodal cells are often very prominently associated
with the haustorial apparatus for obtaining nutritive supplies
from or through the chalazal region. The nutritive function of
the antipodals seems to have been claimed first by Wester-
maier ** 8° in his studies of the prominent antipodals of the
Ranunculaceae. This was confirmed by Osterwalder ® in his
study of Aconitum Napellus; and also by Mlle. Goldflus ®* in
connection with the Compositae. The latest contribution to the
subject is that by Ikeda,1°° in connection with Tricyrtis hirta,
who claims that the antipodals in that species are nutritively
active from the full maturation of the sae to the formation of
endosperm, after which they change in structure and gradually
weaken; and that during that period they not only elaborate
food for endosperm-formation, but also for the growth of the
ege-apparatus. The eutinization of the integument prevents
the passage of materials except by way of the chalaza, and
hence much of the nutrition must pass through the antipodals.
Ikeda describes and figures the position of starch, dextrine,
and eutinized membranes at various stages in the development
of the ovule and embryo (Fig. 52). From this point of view
antipodals are of two general types, that may be spoken of as
the passive and ageressive types. In the passive type the antip-
odals remain active, often become very much enlarged (as
among Ranunculaceae), or even form a mass of tissue (as in

112 MORPHOLOGY OF ANGIOSPERMS

Sparganium), but they are not associated with an invasion of
the chalazal region, and simply receive material from it. This
type is characteristic of Monocotyledons (except Gramineae)

Starch (abundant).

Dextrine.

E ems CUticularized membranes.

Fie. 52.—Tricyrtis hirta. Various stages in development of ovules, embryo-sac, and
embryo, showing the starch, dextrine, and eutinized membranes at different periods,
the sequence being indicated by the letters 4-G.—A fter TREDA,108

and Archichlamydeae (except many Amentiferae). In the
ageressive type, active, and often multiplying antipodals are

associated with the penetration of the chalazal reeion by the

THE FEMALE GAMETOPHYTE 113

antipodal portion of the sac. This type is characteristic of
Sympetalae, perhaps being especially prominent among the
Rubiaceae and Compositae; but it is also conspicuous among
the Gramineae and Amentiferae. Among the Amentiferae it
is noteworthy that an antipodal haustorium occupied by active
antipodal cells and a special vermiform haustorium occupied
by endosperm cells are often both present.

That every suspensor is an haustorium for the embryo
seems evident, but aside from this general fact special out-
growths from the suspensor are developed to reach a wider
range of nutritive supplies. The case of certain orchids whose
suspensors develop vermiform haustoria that envelop the em-
bryo, or grow through the micropyle and embed themselves in
the wall of the ovary, has long been known; and it has been
receutly found that among certain Rubiaceae (Galieae) the
filamentous suspensor sends out conspicuous lateral processes
or branches that penetrate the endosperm (Lloyd 1°).

In some cases a complex mechanism for nutrition has been
described, and numerous others will be discovered when atten-
tion is given to the subject. The case of Phlox Drummondia,
as described by Billings,’°° may be used as an illustration. The
wall of the ovary adjacent to the micropyle develops a papilla
of special structure consisting of elongated cells. This presses
against the micropyle, which becomes closed and resembles con-
ducting tissue. A papilla of small cells develops from the adja-
cent integument in contact with the sac, and pressing into it is
put in connection with the suspensor. In testing this mecha-
nism for starch, Billings found starch in the ordinary tissue of
the ovary wall, no starch in the wall-papilla, and abundant
starch again in the integument bordering the old micropyle.
This seems to establish a definite passage of nutritive supplies
from the ovary wall, through a series of specially developed
tissues, to the suspensor.

Tn Stylidium squamellosum (Burns **) there is a remarkable
combination of nutritive structures (Fig. 50). The micropylar
end of the sae enlarges enormously and spreads out through the
thick integument, a remarkable nutritive jacket of radially
elongated cells invests the lower part of the sac, and a distinct
gland-like nutritive tissue is developed in the chalaza adjacent
to the antipodal end of the sae.

114 MORPHOLOGY OF ANGIOSPERMS

10.

11.

13.

14.

15.

16.

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Monocotyledonous Plants. Bot. Gazette 80: 25-47. pls. 6-7.
1900.

81. Lanp, W. J. G. Double Fertilization in Compositae. Bot. Gazette
30: 252-260. pls. 15-16. 1900.

82. Lotsy, J.P. Rhopalocnemis phalloides Jungh., a Morphological-
systematical Study. Ann. Jard. Bot. Buitenzorg IT. 2: 73-101.
pls. 3-14. 1900.

83. CHopat, R., and BERNARD, C. Sur le sac embryonnaire de IU’ He-
losis guayanensis. Jour. Botanique 14: 72-79. pls. 1-2. 1900.

84. Bernarp,C.H. Recherches sur les spheres attractives chez Lilium
candidum, ete. Jour. Botanique 14: 118-124, 177-188, 206-212.
pls. 4-5. 1900.

85. Burns, G. P. Beitriige zur Kenntniss der Stylidiaceen. Flora 87:
318-354. pls. 13-14. 1900.

86. Cannon, W. A. A Morphological Study of the Flower and Em-
bryo of the Wiid Oat, Avena fatua. Proc. Calif. Aead. Sei. IIT.
1: 329-364. pls. 49-53. 1900.

87. Jounson, D. 8. On the Development of Saururus cernuus L.
Bull. Torr. Bot. Club. 27: 365-872. pl. 23. 1900.

88. JuEL, H. O. Beitriige zur Kenntniss der Tetradenbildung. Jahrb.
Wiss. Bot. 35: 626-659. pls. 15-16. 1900.

89. Dunn, Louise B. Morphology of the Development of the Ovule
in Delphinium exaltatum. Proc. Amer. Assn. Ady. Sei. 49; 284.
1900.

S9a. GUIGNARD, L. L’appareil sexuel et la double fécondation dans
les Tulipes. Ann. Sci. Nat. Bot. VIL. 11: 365-387. pls. 9-11. 1900.

La double fécondation dans le mais. Jour. Botanique
15: 37-50. 1901.

91. Lana, F. X. Untersuchungen tiber Morphologie, Anatomie, und
Samenentwicklung yon Polypompholyx und Byblis gigantea.
Flora 88: 149-206. pl. 12. figs. 80. 1901.

90.

109.

110.

THE FEMALE GAMETOPHYTE 119

2. ROSENBERG, O. Ueber die Embryologie von Zostera marina.

Bih. Handl. Svensk. Vetensk. Akad. 273: no. 6. pp. 26. pls. 2.
1901.

Ueber die Pollenbildung von Zostera. Meddel. Stock-
holms Hogsk. Bot. Inst. pp. 21. 1901.

4. MuRBECK,S. Parthenogenetische Embryobildung in der Gattung

Alchemilla. Lunds Univ. Arsskrift 867: no. 7, pp. 46. pls. 6.
1901.

5, SCHNIEWIND-THIES, J. Die Reduktion der Chromosomenzahl und

die ihr folgenden Kerntheilungen in den Embryosackmutter-
zellen der Angiospermen. Jena. 1901.

j, STRASBURGER, E. Einige Bemerkungen zu der Pollenbildung bei

Asclepias. Ber. Deutsch. Bot. Gesell. 19: 450-461. pl. 24. 1901.

. Houtrerty, G. M. Ovule and Embryo of Potamogeton natans.

Bot. Gazette 31: 339-346. pls. 2-3. 1901.

. ScHAFFNER, J. H. A Contribution to the Life-History and

Cytology of Erythronium. Bot. Gazette 31: 369-387. pls. 4-9.
1901.

. Frye, T. C. Development of the Pollen in some Asclepiadaceae.

Bot. Gazette 32: 325-331. pl. 13. 1901.

0. Bituinas, F. H. Beitrige zur Kenntniss der Samenentwicklung.

Flora 88: 253-318. 1901.

. ATKINSON, G. F. On the Homologies and Probable Origin of the

Embryo-sac. Science 13: 530-538. 1901.

. SMITH, AMELIA C. The Structure and Parasitism of Aphyllon

uniflorum Gray. Contrib. Bot. Lab. Univ. Penn. 2: 111-121.
pls. 13-15, 1901.

. SCHNEGG, H. Beitrage zur Kenntniss der Gattung Gunnera.

Flora 90: 161-208. figs. 28. 1902.

. OLIVER, F. W. On a Vascular Sporangium from the Stephanian

of Grand ’Croix. New Phytologist 1: 60-67. pl. 1. 1902.

5. Luoyp, F. E. The Comparative Embryology of the Rubiaceae.

Mem. Torr. Bot. Club 8: 27-112. pls. 8-15. 1902.

. IkepA, T. Studies in the Physiological Functions of Antipodals

and Related Phenomena of Fertilization in Liliaceae. 1. Tvri-
cyrtis hirta. Bull. Coll. Agric. Imp. Univ. Tokyo 5: 41-72.
pls. 3-6, 1902.

. GUIGNARD, L. La double fécondation chez les Solanées. Jour.

Botanique 16: 145-167. figs. 45. 1902.

. STRASBURGER, E. Ein Beitrag zur Kenntniss von Ceratophyllum

submersum und phylogenetische Erérterungen. Jahrb. Wiss.
Bot. 87: 477-526. pls. 9-11. 1902.
Hauu, J.G. An Embryological Study of Limnocharis emargi-
nata. Bot. Gazette 33: 214-219. pl. 9. 1902.
Overton, J. B. Parthenogenesis in Thalictrum purpurascens.
Bot. Gazette 33: 363-875. pls. 12-15. 1902.
9

116.

MORPHOLOGY OF ANGIOSPERMS

. Wess, J. E. A Morphological Study of the Flower and Embryo

of Spiraea. Bot. Gazette 33: 451-460. figs. 28. 1902. For cor-
rection of names see REHDER in Bot. Gazette 84: 246. 1902.

. DucamP, L. Recherches sur lembryogénie des Aralacées. Ann.

Sci. Nat. Bot. WIIT. 15: 311-402. pls. 6-13. 1902.

3. MurBECK, 8. Ueber Anomalien im Baue des Nucellus und des

Embryosackes bei parthenogenetischen Arten der Gattung Al-
chemilla. Lunds Univ. Arsskrift 387: no. 2. pp. 10. pl. 1. 1902.

. Jonnson, D. 8S. On the Development of Certain Piperaceae.

Bot. Gazette 34: 321-340. pls. 9-10. 1902.

5. KarstEN, G. Ueber die Entwicklung der weiblichen Blithen

bei einigen Juglandaceen. Flora 90: 316-333. pl. 12. 1902.
Ernst, A. Chromosomenreduction, Entwicklung des Embryo-

sackes und Befruchtung bei Paris quadrifolia L. und Trillium

grandiflorum Salisb. Flora 91: 1-46. pls. 1-6. 1902.

. Enpriss, W. Monographie von Pilostyles ingae (Karst.) (Pilo-

styles Uiet Solms-Laub.). Flora 91: 209-236. pl. 20. figs. 29.
1902.

. Frye, T. C. A Morphological Study of Certain Asclepiadaceae.

Bot. Gazette 34: 389-413. pls. 15-15, 1902.
The Embryo-sae of Casuarina stricta. To be published
in Bot. Gazette 35: 1903.

. Ferraris, T. Ricerche embriologiche sulle Ividaceae. I. Em-

briologia del G. Romulea Maratti. Ann. R. Istit. Bot. Roma 9:
221-241. pls. 6-7. 1902.

. JUEL, H.O. Zur Entwicklungsgeschichte des Samens von Cyno-

morium. Beih. Bot. Centralbl. 13: 194-202. figs. 5. 1902.

. SHIBATA, K. Experimentelle Studien iiber die Entwickelung des

Endosperms bei Monotropa. (Vorliufige Mitteilung.) Biol.
Centralbl. 22: 705-714. 1902.

CHAPTER VI

THE MALE GAMETOPHYTE

Tue reduced number of chromosomes appears at the first
mitosis in the pollen mother-cell, which is therefore the first
gametophytic cell (Fig. 53). In every case, so far as known,
two divisions occur in rapid succession, giving rise to four
microspores. Strasburger* bas called attention to the two
modes of division. In one case, most frequent among Mono-
cotyledons, a wall follows the first nuclear division, dividing
the mother-cell into two hemispherical cells; the second nuclear
division is also followed immediately by the formation of a
wall, making two equal cells from each of the hemispheres (Fig.
54). In the other case, more characteristic of the Dicotyledons,
the two nuclear divisions occur before any walls are formed,
all the walls being then formed simultaneously and in such a
way that each of the four cells has the form of a triangular
pyramid with a spherical base—that is, each cell is the quadrant
of a sphere (Figs. 55,56). The former method has been called
successive, the latter simultaneous division. The two modes
are not sharply characteristic of the two great groups of Angio-
sperms, but the successive method is dominant among Mono-
cotyledons and the simultaneous among Dicotyledons. In any
event the result is a tetrad, a group of four cells each of which
is a microspore. In successive division there is a bilateral ar-
rangement of the microspores, and in simultaneous division the
arrangement is tetrahedral; but both arrangements sometimes
occur in the same sporangium.

The arrangement of the tetrad is not always restricted to
these two methods (Fig. 57). Wille?® has described varying
arrangements of microspores in the tetrads of species of Juncus
and Orchis mascula; and in Typha Schaffner ** not only found

121

122 MORPHOLOGY OF ANGIOSPERMS

the tetrads indiscriminately tetrahedral or bilateral, but fre-

quently the four spores are in a row. A tetrad consisting of
: 7 Ctpad ner Of «

four spores in a row has also been found by Strasburger °* and

Fie. 53.—Lilium Martagon. A, transverse section of young microsporangium, showing
two nuclear mitotic figures in sporogenous cells and one in a hypodermal cell; such
figures show 24 chromosomes, the sporophyte number; x 200. B, chromosomes of
a mitotic figure in the wall of a microsporangium, showing 24 chromosomes; x 600.
C, pollen mother-cell; polar view of the first mitosis, showing 12 chromosomes, the
gaumetophyte number, in the nuclear plate; the segments are double, one-half of
each segment will pass to each pole; x 62

D, later stage in first mitosis showing
i 12 chromosomes, each chromosome representing one-half of one of the 12 segments
shown in (; x 625.—After Guianarp.1®

by Frye °° to oceur regularly in Aselepias and allied genera; by
Rosenberg *7 in Zostera; and Neoltia nidus-avis is cited by
Goebel 16 (p. 368).

It has been claimed that in Zostera, Cyperaceae, Clematis,
Helianthemum, Epilobium, Asclepias, and Lappa, only one
microspore is formed by a mother-cell. In every ease except

THE MALE GAMETOPHYTE . 123

Zostera, Cyperaceae, and Asclepias the claim was disproved
long ago; and even these have now been cleared up, so that no
case is known in which a pollen mother-cell becomes a micro-
spore directly without the tetrad divisions. It does not seem
improbable that such a case may exist, for cases of oogenesis

Fie. 54.—Fritillaria persica. Sections showing the two nuclear divisions by which four
microspores are formed in the mother-cell by the successive (bilateral) method;
x 530. A, very young mother-cell; B, nucleus in synapsis; C, 12 chromosomes,
one of them rather indistinct, within the nucleus; D, mitofie figure of the first
division showing the short, thick chromosomes characteristic of the reduction
division; /, later stage of first division, showing vertical view of the 12 chromo-
somes; J side view of same stage showing 12 chromosomes passing to the upper
pole, only 10 for the lower pole being in sight; G, formation of wall between
daughter nuclei; /Z, second division; /, formation of walls.—After StRaAsBURGER.1°

like that of Liliwm are not rare, where the mother-cell gives
rise directly to a single megaspore. As stated, in 1886 Wille *®
found no tetrad in Asclepias syriaca; and in 1892 Chau-
veaud *° observed the reduction division of the pollen mother-

124 MORPHOLOGY OF ANGIOSPERMS

cells of Cynanchum, but seems not to have noted the formation
of a tetrad: but the tetrad, consisting of a row of four micro-
spores, and referred to above as discovered by Strasburger and
by Frye in 1901 in a number of species of Asclepias and in
Cynanch um, was so unusual as to disguise its tetrad nature, and

Fic. 55.—Podophyllum peltatum. Mitosis in pollen mother-cell. 4, telophase of first
division; B, late anaphase of second division; C, telophase of second division; the
nuclei of the four microspores are formed, but the cell walls, as is characteristic of
simultaneous division, have not yet appeared.—After Morrtrer.*

besides, the enlargement and consequent readjustment of the
spores soon break up the row (Fig. 58). The first record of
the occurrence of a tetrad in Asclepias seems to have been made
by Stevens #1 in 1898; and the fourth independent discovery
of it was by Gager ®® in 1902. Elving,’ Wille,’® and Stras-
burger 1? showed that in various species of the Cyperaceae a
tetrad is formed although only one microspore becomes func-
tional, the other soon disorganizing. Juel °° has recently made
a thorough study of Carex acuta (Fig. 59). He finds that the
two characteristic nuclear divisions take place, and that a
cell-plate is formed at each division. The cell-plates are soon
resorbed, however, so that the four nuclei lie free within the
wall of the mother-cell. Three of the nuelei then disintegrate,
while the fourth beeomes the nueleus of the single functional
microspore; and the wall of the mother-cell, inclosing the four
nuclei, becomes the wall of the microspore. In Zostera marina
Rosenberg °? has described the tetrad division of the remarkably
elongated mother-cell (Fig. 11). The divisions are longitudinal
and in parallel planes, resulting in four remarkable filiform

THE MALE GAMETOPHYTE 125

microspores lying side by side, and measuring 3 by 2,000 «
when mature. That this is a tetrad is evident from the rapid
succession of the divisions, the reduction of chromosomes, and
the formation of four spores from a mother-cell.

In some cases a mother-cell may give rise to less than four
microspores, or may produce more than the normal number
(Fig. 60). In 1886 Wille?® summarized the work of previous
investigators, notably of Hofmeister, Tangl, Wimmel, and
Tschistiakoff, and added the results of his own investigations.
The following lists are made :
up largely of forms investi-
gated by Wille himself:

Two microspores from
a mother-cell are occasion-
ally found in Convallaria
multiflora, Asparagus offi-
cinalis, Aconitum Napellus,
Euphorbia Lathyrus, Be-
gonia sp., Saxifraga caespi-
tosa, Azalea indica, and
Syringa vulgaris.

Three microspores were
found in Begonia sp., Saxi-
fraga caespitosa, Azalea in-
dica, and Lonicera coerulea,

Five microspores were
found in Funkia ovata, Fi-
caria vranunculoides, sStel-

war 9 Y * >
larin glauca, Seleranthus Fic. 56.—Scrophularia nodosa. Section of mi-
ANNUUS, Prunus Cerasus, crosporangium showing appearance of spores
Rumex Patientia, Azalea dinthied: (by: Wiig: sumautianegae Tiesnony We
ee : inner tapetum of microsporangium consists
indica, Lonicera coer uled, of greatly elongated cells which are very
Syringa persica, and Sym- glandular in appearance. x 275.
phytum officinale.

Six microspores were found in Hemerocallis fulva, Ficaria
ranunculoides, Elatine hexandra, Cornus sanguinea, Lonicera
coerulea, and Fuchsia sp.

‘ : : : : hei

Seven microspores were counted with certainty in Fuchsia
sp. and fourteen are reported rather doubtfully; eight is given

for Azalea indica, and eight to twelve for Lonicera coerulea,

126 MORPHOLOGY OF ANGIOSPERMS

but it was not absolutely certain that in case of the higher num-
bers all the microspores came from the same mother-cell. In
Hemerocallis fulva Strasburger *° has counted nine microspores
from a single mother-cell; and later Juel#* and Fullmer ** re-
ported six to eight in the same species. More recently Miss
Lyon *° has found five or six microspores of equal size produced
by a single mother-cell of Huphorbia corollata.

According to Wille, two microspores result from a failure
of the mother-cell to undergo the second division. When three
are formed, the first division is unequal, and only the larger
cell divides. Five or
more microspores are
formed by subsequent
division of one or more
members of the tetrad.

Strasburger,?? Juel,?%
and Fullmer,** in their
study of Hemerocallis
fulva found an explana-
tion of the irregular
numbers. — Strasburger
found that chromosomes
which fail to pass to
either pole at the first
mitosis give rise to small

microspores. Juel in his
Fie. 57.—Variation in the arrangement of the spores more reeent study con-
of a tetrad. A-C, Orehis mascula, x 380; after cS :
Witret® D-2, Typha latifolia, x 400; after
Scnarrner.s finds that even single

firms Stra sburger, and

chromosomes which be-
come separated may divide and give rise to nuclei and organize
cells. Fullmer attributes the supernumerary microspores to the
division of one or more members of the tetrad.

Perhaps no phase of plant cytology has received so much
attention as the nuclear divisions in the pollen mother-cell. It
is an interesting fact that the cytological characters of these two
mitoses agree minutely with those in the megaspore mother-
cell. The pollen mother-cell ean be positively identified by the
appearance of the synapsis stage (Fig. 54, B), even before any
rounding off or separation takes place. While yet in the spirem

E

Fie. 58.—Development of male gametophyte in Aselepias. A-D, A. Cornuti; C-E, A.
tuberosa. A, section of young microsporangium showing archesporial cells; B,
portion of the single layer of elongated mother-cells; C, later stage showing two
mother-cells, the lower one dividing and showing 10 chromosomes, the gametophyte
number; D, second division of mother-cell, by which the row of four microspores is
formed; £, microspore showing tube nucleus (¢) and generative nucleus (g). A,
x 200; B-L, x 800.—After Frye.

127

128 MORPHOLOGY OF ANGIOSPERMS

stage the chromatin thread splits longitudinally throughout its
entire leneth (Fig. 61, 41, 2). The double thread then seg-
ments transversely into the number of chromosomes characteris-

Fie. 59.—Development of microspores in Heleocharis palustris and Carex acuta. A-B,
Heleocharis:

spores, x

, showing the single functional microspore and three disorganizing micro-
; after STRASBURGER.!2 C-J, Carex

8 C,mother-cell ; D, second division;
F, four nuclei, only three of which are shown within the mother-cell (# and F
should be reversed); £, later stage than /’; the nucleus of the functional micro-
spores is preparing for division; G, tube nucleus, generative cell, and lower down
the nuclei of the three non-functional microspores ; /Z, nearly ripe pollen grain; J,
irregular case in which the nuclei of the three non-functional microspores have
divided; x 900.—After JuEL.5° :

tic of the gametophyte of a given species, each chromosome thus
being made up of two pieces (Fig. 53, C). According to several
investigators, a second longitudinal splitting of the chromo-
somes may be seen during the anaphase of the first mitosis, so
that the two mitoses merely distribute the reduced number of
chromosomes which appear just after the segmentation of the
spirem. In the subsequent mitoses the spirem segments into
chromosomes which afterward split longitudinally as in vege-
tative cells.

It is in the divisions of the pollen mother-cell that the
problem of the reduetion of chromosomes has been studied most
thoroughly; but while it is agreed that the reduced number
appears at the first mitosis, there is still some difference of

H

THE MALE GAMETOPHYTE 29
opinion as to whether a qualitative division occurs. At present
the weight of evidence is against such a division.

According to nearly all recent observers (Belajeff,24 Stras-
burger,”* Mottier,?* Lawson,** Miss Byxbee *?) the spindle in
the first mitosis originates as a multipolar structure, which

D

Fie. 60.—Microspore mother-cells producing more or less than four microspores. A-B,
Hemerocallis fulva, with five and eight microspores in process of formation ;
A x 1000; Bx 625; after Jue. C, Luphorbia corollata, with five microspores
of equal size within mother-cell; x 625; after Lyon.10 D, Begonia sp., with three
microspores from a mother-cell; x 400. £, Ficaria ranuneuloides, with six micro-
spores, x 400. F, Azalea indica, with six microspores, three having come from the
division of one of the spores of the tetrad, x 400. D-&, after WILLE.16

gradually becomes bipolar (Figs. 61, 61a). In a few cases mul-
tipolar spindles have been described for the second mitosis. In
vegetative cells the spindle first appears as a pair of dome-
shaped prominences or caps. Transitions between the two

modes are not lacking.

130 MORPHOLOGY OF ANGIOSPERMS

The number of chromosomes observed in connection with
the reduction division have been noted in the preceding chap-
ter (p. 81).

Fra. 61.—First division of pollen mother-cell, showing formation of the bipolar from the
multipolar spindle. 4, B, 2, F, Lilium Martagon, C-D, L. candidum, A, double
row of chromatin granules upon the linin thread ; ZB, later stage in which the entire
thread has split longitudinally ; C, formation of a weft of fibers about the nucleus;
DPD, multipolar spindle; /, bipolar spindle; F, telophase of first division showing
that the division is of the successive type.—After Morripr.2¢

THE MALE GAMETOPHYTE 13

After the two divisions, each of the four young microspores
becomes invested by a delicate wall which is independent of the
common wall of the mother-cell. This wall soon becomes differ-
entiated into two layers, the inner one (intine) consisting of
pure cellulose and later developing the pollen-tube.

The outer layer (exine) is eutinized, and especially among
Dicotyledons becomes variously sculptured, often being covered
with ridges, warts, spines, ete., as fully described by Schacht ?
and Luerssen.® For the most part, there are thin spots in the
exine for the exit of pollen-tubes. It is interesting to note that
only a single point of exit occurs in the microspores of most
Monocotyledons and of a few Dicotyledons; while in most Di-
cotyledons there are from two to many such points of exit.
Goebel ?® (p. 367) has given the following
illustrations from Schacht: two points of
exit in Ficus, Justicia, ete.; three in Cupu-
liferae, Praarcne Ger raniacese, Onagra-
ceae, Boraginaceae, and Compositae; four
to six in Alnus, Carpinus, Astrapaea, and
Impatiens; many in Alsineae, Malvaceae,
Convolvulaceae, ete. Barnes!? records is :

: 4 : Fic. 61a.—Lilium candi-
three to twelve thin spots in the exine of gum. Multipolarspin-
Campanula, and Coulter *” finds fifteen to dle at first division
thirty such areas in that of Ranunculus. — %f Pollen mother-cell,

. ee x 400.— After Brxa-
In certain cases a much more specialized — jgppas
method for the exit of the pollen-tube is
provided, as among the Cucurbitaceae and in Passflora, in
which pemuaieh, lid-like, and often embossed pieces of the exine
become detached; and in Thunbergia, in which the layer of
exine splits into exfoliating spiral bands. Among those aquatics
that pollinate under water, as well as in the pollinia-bearing
forms, the exine,4#s said to be lacking. The origin and devel-
opment of the walls of spores is a problem that needs further

investigation.

For the most part, the microspores become entirely free
from one another at maturity, forming a pulverulent mass, but
there are instances of microspores failing to pero dissociated,
giving rise to the so-called “ compound grains” (Figs. 13, byO}s
In the simplest cases the four spores of a tetrad cling together,
as in Typha, certain orchids (as Neottia), Anona, Hoarca

132 MORPHOLOGY OF ANGIOSPERMS

and Rhododendron; in other cases the whole product of a
primary sporogenous cell, ranging from eight to sixty-four
microspores, clings in a mass, as the massulae of certain orchids
(Ophrydeae) and the groups of pollen-grains found among the
Mimoseae; and in the most extreme cases, the whole product
of a sporangium forms a single mass, the polliniwm, character-
istic of certain Orchids and of the Asclepiadaceae. It is of
interest to note that all of these conditions occur among Or-
chidaceae, from isolated microspores (Cypripedium) to the com-
pletely organized pollinium. Such variations and others have
been described in detail by Reichenbach,! Hofmeister,* Rosa-
noff,* Corry,!? and others.

The older botanists were not able to recognize the structures
developed within the mature pollen-grain, whose contents they
called “ fovilla,” regarding it as a fertilizing substance rich in
food material In 1878 Strasburger® discovered that struc-
tures are developed in the microspores of Angiosperms com-
parable to those already known in Gymnosperms, and this was
confirmed by Elfving.*

The germination of the microspore begins with the division
of its nucleus, and this always occurs before dehiscence, some-
times long before, the two daughter nuclei having been found
even in midwinter, as in Alnus and Corylus (Chamberlain 35)
(Fig. 8). When first formed, the daughter nuclei are usually
alike in size and form, but in most cases the tube nucleus soon
becomes much larger, the differentiation sometimes beginning,
as in Cypripedium, before the mitosis is fully completed (Fig.
62). In any case, the nuclei soon become differentiated, the
tube-nucleus having a large nucleolus and a rather seanty chro-
matin network; while the generative nucleus is smaller, has a
smaller nucleolus or none at all, and its chromatin is denser
and less irregular. The nuclei also differ in their reaction to
stains, a combination like eyanin and erythrosin staining the
tube-nucleus red and the generative nucleus blue.

At first Strasburger® thought that the tube-nuclens was
concerned not merely in developing the pollen-tube, but also in
fertilizing the egg, and hence named it the “ generative nu-
cleus.” The other nucleus, although seen to enter the tube and
even divide, was thought to take no part in the processes con-
nected with fertilization, and was called the “ vegetative” or

THE MALE GAMETOPHYTE 133

“prothallial” nucleus. This older view is the one given in
Goebel’s Outlines of Classification and Special Morphology. In
1884 Strasburger !? recognized the real nature of the two nuclei
and interchanged the names, applying them as they have been
used ever since. We have substituted the name “ tube-nucleus ”
for “ vegetative nucleus,” not only because the development of
the tube is its most conspicuous function, but also because it is

es a #, o® hs Fe “”

Fie. 62.—Cypripedium spectabile. Section of microsporangium, showing microspores in
various stages of division into tube and generative nuclei; although the divisions
are nearly simultaneous throughout the microsporangium, it will be seen that in
some cases the nuclei are in the spirem stage, while in others the tube and genera-
tive nuclei are easily distinguished; x 300.

not the morphological equivalent of the vegetative or prothallial
cells of the Gymnosperms and heterosporous Pteridophytes.

A generative cell is formed by the more or less distinct or-
ganization of the cytoplasm about the generative nucleus. This
cell usually lies free in the body of the spore, but is often cut
off by a distinct wall, as in Typha (Schaffner *"), Sparganium
(Campbell ##), Natas (Campbell **), Convallaria (Wiegand *°),
Neottia (Guignard®), Populus (Chamberlain *°), Asclepias

184 MORPHOLOGY OF ANGIOSPERMS

(Frye *°), and Sarcodes (Oliver?*). Both methods are often
found in the same species and even in the same anther, as in
Lilium (Fig. 63).

The free generative cell finally assumes a variety of forms,
the most common being lenticular, the cytoplasm massing chiefly

Fro. 63.—Male gametophyte at time of shedding. B, C, Lilinm auratum; the others
L. tigrinum; x 500. A, generative cell against side of microspore ; B, generative
cell in body of microspore; the two male nuclei already formed; C, three male
nuclei within generative cell, an unusual case: D, two male nuclei, differing in size,
within generative cell; 2, tube-nucleus divided, giving rise to six nuclei; F, an
unusual case, showing tube-nucleus, two generative cells (7), and a “ prothallial”
cell (pr).—After CHAMBERLAIN,®2

at two opposite poles of the nucleus. In some cases a spherical
form is maintained, as in Acer (Mottier “2; in others the len-
ticular form passes into the vermiform, becoming elongated and

THE MALE GAMETOPHYTE 135

even coiled or twisted, as in Vradescantia (Coulter and
Rose **) ; or the cytoplasm of the spindle-shaped generative cell
may taper into elongated whip-like filaments that more or less
encircle the tube-nucleus, as in Hichhornia (Smith*®). In
ELrythronium Schafiner °° found that the generative nucleus is
larger than the tube nucleus and is surrounded by a densely
staining amoeboid-torm mass of cytoplasm. It is altogether
probable that the size and form of free generative cells varies
with age and external conditions, so that they may be relatively
large or small; or spherical, lenticular, spindle-shaped, or ver-
miform in the same species. It is very common to find them at
first spherical and later lenticular, as has been frequently ob-
served in Lilium.

in Lilium tigrinum Chamberlain ** often found a small cell
cut off by the microspore before the appearance of the tube and
generative nuclei, and the same cell was noted after the division
of the generative nucleus (Fig. 63). A similar cell was found
by Smith *? in Hichhornia crassipes and by Campbell ** in Spar-
ganium simplex. It is suggestive of a true vegetative or pro-
thallial cell, two of which so commonly occur among the Gym-
nosperms; but the phenomenon is too unique as yet among
Angiosperms to deserve more than a mention.

The tube-nucleus usually increases much in size, and under
certain conditions has been found to fragment, as in Lilium, in
which Chamberlain ** found four and in one case eight tube-
nuclei; in Hichhornia, in which Smith *® found two tube-nuclei
in half the pollen-grains examined; in Hemerocallis, in which
Fullmer ** reports the frequent occurrence of two to six tube-
nuclei; and in Asclepias, in which Frye °° observed a fragment-
ing nucleus. This phenomenon is doubtless not uncommon in
certain conditions of nutrition.

The generative nucleus or cell may divide in the pollen-
erain, even long before dehiscence, as in Sagittaria (Schaff-
ner *!); or the generative cell may pass into the tube before
division, sometimes not dividing until immediately before fer-
tilization. The time of this division seems to hold no relation
to the great plant groups, and may be variable in the same genus
or even species. For example, in Lilium tigrinum it often
takes place in the grain, but in L. philadelphicum rarely so;
and in this last species it may occur either in the grain or at

10

186 MORPHOLOGY OF ANGIOSPERMS

any time in the tube up to its completed growth. The variable
relation of the time of this division to the great groups may be
illustrated by the following record :

Among Monocotyledons the generative nucleus divides in
the pollen-grain in Potamogeton CW iegand *°), Alisma ( Sehatt-
ner 75), Sagittaria ( Schaffner *+), Avena (Cannon 28) Mab
cum and other grasses (Golinski *+), Lemna (Caldwell #7), and
Lilium (Chamberlain ®2); and in the pollen-tube in Symplo-
carpus (Duggar #7), T'radescantia (Coulter and Rose 1+), Bich-
hornia (Smith#®), Lilium (Chamberlain **), Convallaria

(Weigand a Erythronium (Schaffner **), and the Orchids
(Guignard ®). In examining this record it might be concluded
that the ete division of the generative cell within the pollen-
grain is a more primitive deamauien in general than the later
division in the pollen-tube. Even if this should prove to be
true for the Monocotyledons, it can hardly be claimed for the
Dicotyledons, as the following record shows:

Among Dicotyledons the generative nucleus or cell divides
in the pollen-grain in Rhopalocnemis (Lotsy *1), Papaver,
Hesperis, Archangelica, and Mertensia (all by Strasburger **),
Nicotiana Tabacum (Guignard*®), Sambucus (Halsted),
and Silphium (Merrell #5); and in the pollen-tube in Pe pero-
sae Johnson #°), Salix (Chamberlain °°), Ranunculus (Coul
ter *7), Lathyrus (Strasburger !*), Buphorbia (Mass Lyon *),
ae (Strasburger 1"), Acer (Mottier **), Vinca, Nemo-
phila, Digitalis, and Torenia (all by Strasburger !*), Campa-
nula (Barnes!*), and Datura laevis (Guignard**). It is
evident that the two conditions are found among Dicotyledons
in both primitive and high groups, and even in the same family
(as Solanaceae), and that neither one has any claim to be
regarded as an essentially primitive character.

The male nuclei, formed by the division of a generative nu-
cleus, are possibly always associated with eytoplasm in such
a way that definite male cells are organized. The nucleus is
often the only conspicuous feature, and in every ease it finally
constitutes the bulk of the male cell. In fact, in most of the
plants studied only the male nueleus has been demonstrated in
the pollen-tube and embryo-sac. In the following citations
“male nucleus ” and “ male cell” are used to indicate whether
cytoplasm was demonstrated or not. Various forms of male

THE MALE GAMETOPHYTE 137

cells and nuclei have been described, but it is evident that the
form as well as the size may change decidedly in the course of
its history. For example, Schaffner * notes that the male nuclei
in Sagittaria are at first spherical, but after pollination become
bean-shape or spindle-shape. In Si/phium Merrell #8 observed
the originally spherical male nuclei become much elongated, more
or less curved, and even spirally twisted while still within the
pollen-grain (Fig. 64); and in Triticum and other grasses Go-
linski *! implies the same changes in
form in describing the occurrence of
a nuclei within the pollen-grain
as “not unlike the antherozoids of a
fern or of Chara.’ Tt has been re-
peatedly observed that the spherical
nuclei of the oblong or lenticular
male cells of Liliwm inerease in size
and become vermiform and variously
curved and coiled after discharge
from the pollen-tube, and the same
phenomenon was observed by Miss
Thomas ** in Caltha.

It seems to be generally true it
the male cells when formed free in
the body of the grain are at first
spherical, but soon become oblong or Rye, 64,—.4, microspore of Silphi-
lenticular. In a forthcoming paper — wmintegrifolium,showing tube-
by Koernicke it will be shown that in aoe oe ae oe
Inlium only male nuclei are found in — cewm, showing, the two male
the poilen-tube; at least there are no — cells. @, single male cell of SS.
male cells as ordinarily figured. This ees ike aatinae as
claim is of special interest, since in
Lilium male cells are clearly organized in the pollen-grain.
The increase in size and change of form so often described as
taking place in the tube or sac are probably phenomena of the
male nucleus rather than of the male cell. There are well-
known cases, however, in which the spherical or oblong form
persists throughout the history of the nucleus. For example, in
Peperomia (Johnson *°) the male nucleus is spherical even in
contact with the egg, and the same is true of several other forms
recently investigated in connection with double fertilization.

138 MORPHOLOGY OF ANGIOSPERMS

There is also indication that the two male nuclei may be-
eome differentiated in form, as in the case of Alisma, in which
Schaffner 28 found the upper male nucleus in the pollen-tube
elongated or spindle-shaped, and the lower one spherical. It
is also probable that in cases of double fertilization the two
male nuclei often assume different forms in the embryo-sac.
Four male nuclei have been reported by Strasburger ** as some-
times occurring in Camassia Fraseri, and Chamberlain ** has
observed three nuclei within a single male cell in Lilium aura-
tum (Fig. 63, C). This recalls the spermatogenesis of Gymno-
sperms, in which the generative cell gives rise to a stalk cell
and two male cells, but it may have no further significance
than that any active cell may be induced to divide by favorable
conditions. ;

The morphology of the structures included in the male
gametophyte of Angiosperms is obscure. In 1884 Stras-
burger 1? suggested that only an antheridinm is developed
within the pollen-grain, the vegetative or prothallial tissue, rep-
resented in many Gymnosperms, having been entirely sup-
pressed. The same view has been developed in several papers
from this laboratory, and in 1898 Belajeff*® reiterated it in
a discussion including both Gymnosperms and Angiosperms.
According to this view, the larger tube-cell is the antheridium
wall that develops ‘a tubular outgrowth, used at least in Angio-
sperms as the carrier of the male nuclei, while the generative
cell and its product is the spermatogenous part of the antherid-
ium. It is not exact to say that according to this view the
whole pollen-grain is an antheridium, but that in its germina-
tion the pollen-grain develops only an antheridium.

Another view, which seems to be the only alternative, is
that while only an antheridium is present its sole representative
is the generative cell, the tube-cell not being any more a part
of the gametophyte than is the embryo-sac. The divergence
between the two views, therefore, has to do only with the nature
of the tube-cell. In any event, it is important to note, as contra-
dicting a very common statement, that the pollen-tube is not the
male gametophyte.

The development of the pollen-tube and the passage of the
male nuclei to the embryo-sae are so directly connected with
fertilization that they will be considered in the next chapter.

wx

[o2)

10.

11.

12.

THE MALE GAMETOPHYTE 139

LITERATURE CITED

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et de Orchideis in artem ac systema regigendis. Leipzig. 1852.

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Bot. 2: 107-168. pls. 14-18. 1860.

. Hormeister, W. Neue Beitriige zur Kenntniss der Embryo-

bildung der Phanerogamen. Abhandl. Ko6nig]. Sachs. Gesell.
Wiss. 6: 533-672. pls. 1-27. 1859.

. Rosanorr, 8. Zur Kenntniss des Baues und der Entwicklungsge-

schichte des Pollens der Mimoseae. Jahrb. Wiss. Bot. 4: 441-
450. pls. 31-32. 1865.

. LuERSSEN, C. Zur Controverse iiber die Einzelligkeit oder Mehr-

zelligkeit des Pollens der Onagrarieen, Cucurbitaceen und Cory-
laceen. Jahrb. Wiss. Bot. 7: 34-60. pls. 3-5. 1869.

. STRASBURGER, E. Befruchtung und Zelltheilung. Jena. 1877.
. ELFVING, F. Studien tiber die Pollenkérner der Angiospermen.

Jenaisch. Zeitsch. Naturwiss. 18: 1-28. 1879; Quart. Jour. Micr.
Sci. 20: 19-35. 1880.

. STRASBURGER, E. Zellbildung und Zelltheilung. Ed. 3. Jena.

1880.

. GUIGNARD, L. Recherches sur le développement de l’anthére et

du pollen des Orchidées. Ann. Sci. Nat. Bot. VI. 14: 26-45. pl.
2. 1882.

STRASBURGER, E. Ueber den Theilungsvorgang der Zellkerne und
das Verhiltniss der Kerntheilung zur Zelltheilung. Archiv. Mikr.
Anat. 21: 476-590. pls. 25-27. 1882.

Corry, T. H. Structure and Development of the Gynostegium,
ete., in Asclepias Cornuti. Trans. Linn. Soc. Bot. London
2: 173-207. pls. 24-26. 1884.

STRASBURGER, E.: Neue Untersuchungen iiber den Befruchtungs-
vorgang bei den Phanerogamen. Jena. 1884.

. Barnes, C. R. The Process of Fertilization in Campanula amer-

icana. Bot. Gazette 10: 349-354. pl. 10. 1885.

. CouLTeR, J. M.,and Ross, J. N. The Pollen Spore of Tradescantia

virginica. Bot. Gazette 11: 10-14. pl. 1. 1886.

. WixLE, N. Ueber die Entwickelungsgeschichte der Pollenkérner

der Angiospermen und das Wachsthum der Membranen durch
Intussusception. Christiania. 1886.

. GOEBEL, C. Outlines of Classification and Special Morphology.

English translation. 1887.

7. Hausrep, B. D. Three Nuclei in Pollen Grains. Bot. Gazette 12:

285-288. pl. 16, 1887.

. OLIVER. F. W. On Sarcodes sanguinea. Annals of Botany 4:

303-826. pls. 17-21. 1890.

140 MORPHOLOGY OF ANGIOSPERMS

33.

34.

. GUIGNARD, L. Nouvelles études sur la fécondation. Ann. Sci.

Nat. Bot. VII. 14: 163-296. pls. 9-18. 1891.

. CHAUVEAUD, G. L. Sur la fécondation dans les cas de polyembry-

onie. Compt. Rend. 114: 504. 1892.

. GOLINSKI, St. J. Ein Beitrag zur Entwicklungsgeschichte des An-

droeceums und des Gynaeceums des Griiser. Bot. Centralbl. 55:
1-17, 65-72, 129-135. pls. 1-3. 1893.

. Mottier, D. M. Development of the Embryo-sae in Acer rubrum.

Bot. Gazette 18: 3875-377. pl. 34. 1893.

3. Humpurey, J. E. Nucleolen und Centrosomen. Ber. Deutsch.

Bot. Gesell. 12: 108-117. pl. 6. 1894.

. BELAJEFF, W. Zur Kenntniss der Karyokinese bei den Pflanzen.

Flora. Ergaénzungsband, 1894.

. STRASBURGER, E. Karyokinetische Probleme. Jahrb. Wiss. Bot.

28: 151-204. pls. 2-3. 1895.

. Mortier, D. M. Beitrage zur Kenntniss der Kerntheilung in den

Pollenmutterzellen einiger Monokotylen und Dikotylen. Jahrb.
Wiss. Bot. 30: 169-204. pls. 5-5. 1897.

. CAMPBELL, D. H. The Structure and Development of the Mosses

and Ferns. London and New York. 1895.

. SCHAFFNER, J. H. The Embryo-sae of Alisma Plantago. Bot.

Gazette 21: 123-132. pls. 9-10. 1896.

. CAMPBELL, D. H. A Morphological Study of Naias and Zannichel-

lia. Proe. Calif. Acad. Sci. III. 1: 1-62. pls. 1-5. 1897.

. CHAMBERLAIN, C. J. Contribution to the Life History of Salix.

Bot. Gazette 23: 147-179. pls. 12-18. 1897.

. SCHAFFNER, J. H. Contribution to the Life History of Sagittaria

variabilis. Bot. Gazette 23: 252-273. pls. 20-26. 1897.

. CHAMBERLAIN, C. J. Contribution to the Life History of Liliwm

Philadelphicum ; the Pollen Grain. Bot. Gazette 238: 423-430.
pls. 35-36, 1897.

JureL, H. O. Die Kerntheilungen in den Pollenmutterzellen von
Hemerocallis fulva und die bei denselben auftretenden Un-
regelmissigkeiten Jahrb. Wiss. Bot. 30: 205-226. pls. 6-8.
1897.

ScHAFFNER, J. H. The Development of the Stamens and Carpels
of Typha latifolia. Bot. Gazette 24: 93-102. pls. 4-6. 1897.

- Lawson, A. A. Some Observations on the Development of the

Karyokinetic Spindle in the Pollen Mother-cells of Cobaea
scandens. Proc. Calif. Acad. Sci. III. 1: 169-184. pls. 33-36.
1898.

. BELAJEFF, W. Die verwandtschaftlichen Beziehungen zwischen

den Phanerogamen und den Cryptogamen in Lichte der neues-
ten Forschungen. Biol. Centralbl. 18: 209-218. 1898.

Covtter, J. M. Contribution to the Life History of Ranunculus.
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39.

41.

42.

43.

44,

46.

52.

53.

54.

55.

THE MALE GAMETOPHYTE 141

3. CHAMBERLAIN, C. J. Winter Characters of Certain Sporangia.

Bot. Gazette 25: 124-128. pl. 11. 1898.
SmitH, R.W. A Contribution to the Life History of the Ponte-
deriaceae. Bot. Gazette 25: 324-337. pls. 19-20. 1898.

. Lyon, FLorence M. A Contribution to the Life History of

Euphorbia corollata. Bot. Gazette 25: 418-426. pls. 22-24.
1898.

STEVENS, W.C. The Behavior of the Kinoplasm and Nucleolus
in the Division of the Pollen Mother-cells of Asclepias Cornutt.
Kansas Uniy. Quarterly 7: 77-85. pl. 15. 1898.

CALDWELL, O. W. On the Life History of Lemna minor. Bot.
Gazette 27: 37-66. figs. 59. 1899.

CAMPBELL, D.H. Notes on the Structure of the Embryo-sac in
Sparganium and Lysichiton. Bot. Gazette 27: 153-166. pl. 1.
1899.

FutimeEr, E. L. The Development of the Microsporangia and Mi-
crospores of Hemerocallis fulva. Bot. Gazette 28: 81-88. pls.
7-8, 1899.

. WIEGAND, K. M. The Development of the Microsporangium and

Microspores in Convallaria and Potamogeton. Bot. Gazette 28:
328-359. pls. 24-25. 1899.

Cannon, W. A. A Morphological Study of the Flower and Em-
bryo of the Wild Oat, Avena fatua. Proc. Calif. Acad. Sci. III.
1: 329-364. pls. 49-58. 1900.

. DuGGAR, B. M. Studies in the Development of the Pollen Grain in

Symplocarpus foetidus and Peltandra undulata. Bot. Gazette
29: 81-98. pls. 1-2. 1900.

3. MERRELL, W. D. A Contribution to the Life History of Silphium.

Bot. Gazette 29: 99-133. pls. 3-10. 1900.

. JoHnson, D. 8. On the Endosperm and Embryo of Peperomia

pellucida. Bot. Gazette 30: 1-11. pl. 1. 1900.

. JUEL, H.O. Beitriige zur Kenntniss der Tetradenbildung. Jahrb.

Wiss. Bot. 35: 626-659. pls. 15-16. 1900.

. Lotsy, J. P. Rhopalocnemis phalloides Jungh., a Morphological-

systematical Study. Ann. Jard. Bot. Buitenzorg II. 2: 73-101.
pls. 3-14. 1900.

ByxBEk, EpirH. The Development of the Karyokinetic Spindle
in the Pollen Mother-cell of Lavatera. Proc. Calif. Acad. Sci.
III. 2: 63-82. pls. 10-13. 1900.

THomas, ETHEL M. On the Presence of Vermiform Nuclei in a
Dicotyledon. Annals of Botany 14: 318-319. 1900.

STRASBURGER, E. Einige Bemerkungen zu der Pollenbildung
bei Asclepias. Ber. Deutsch. Bot. Gesell. 19: 450-461. pl. 24.
1901.

Scuarrner, J.H. A Contribution to the Life History and Cy-
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142 MORPHOLOGY OF ANGIOSPERMS

56. FryE, T. C. Development of the Pollen in some Asclepiadaceae.
Bot. Gazette 32: 325-331. pl. 13. 1901.

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Stockholms Hoégsk. Bot. Inst. pp. 21. 1901.

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in Asclepias Cornuti. Annals of Botany 16: 123-148. pi. 7.
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59. GUIGNARD, L. La double fécondation chez les Solanées. Jour.
Botanique 16: 145-167. figs. 45. 1902.

60. CHEAUVEAUD, G. L. De la reproduction chez le dompte-venin.
Diss. Paris. 1902.

CHAPTER VII
FERTILIZATION

Ty various ways the male gametophyte reaches the stigma.
The literature dealing with pollination has become very exten-
sive, and can not even be recapitulated here, especially as it is
an ecological subject. The development of tubes from pollen-
grains lodged upon stigmas has long been known, but the rela-
tion of the tubes to fertilization was long misunderstood. An
historical account of the early views of fertilization among An-
giosperms, together with the citation of literature, was given
by Schacht? in 1850, and by Hofmeister? in 1851. A few
notes from Schacht’s account may not be without interest, and
the reproduction of some of his figures will serve to show the
technique of the time and to illustrate how theories may in-
fluence interpretation (Fig. 65).

In 1681 Malpighi discovered the ovule and the embryo-
sac, and also examined the pollen, but regarded it as a useless
secretion. No important advance was made until 1823, when
Amici discovered the pollen-tube on the stigma of a Portulaca
and succeeded in tracing the tube to the ovule. In 1826 Bron-
eniart traced the pollen-tube in many plants, and in Pepo
macrocarpus saw hanging from the micropyle the end of the
vane that had passed into the embryo-sac; “ but,” says Schacht,

“he misinterpreted the phenomenon, for he mapatded the pol-
len-tube as a fertilizing tube through which the fertilizing con-
tents were brought to the embryo-sac, there to be taken up by
the ‘embryonal vesicle,’ a cell arising in the sac.” In 1826
Robert Brown described the development of the integuments,
and later traced the pollen-tubes of orchids and asclepiads from
the stigma to the micropyle. Jn 1833 the knowledge of the
subject may be summarized as follows: there had been observed

148

144 MORPHOLOGY OF ANGIOSPERMS

the pollen-grain with its pollen-tube and some contents, as well
as the ovule with its integuments and embryo-sac; and the
pollen-tube had been traced from the stigma to the embryo-sae.

Fie. 65.—A-C, Orchis Morio; D, O. latifolia; E, O. maculata; F, Canna limbata.
A-B, young ovules, x 150; C, end of pollen-tube enlarging, x 100; J), later stage
with two nuclei visible in embryo, x 166; £, more advanced embryo, x 208; F,
considerably later stage, x 125.—After Scuacnt.!

In 1835 Schleiden, the founder of the cell-theory, traced
the pollen-tube in a large number of widely separated familhes.
He claimed to have seen the tube enter the micropyle, press ito
the embryo-saec, and then beeome itself the embryonal vesicle,
the beginning of the embryo. He thought that the contents of
the pollen-tube not only give rise to the embryonal vesicle, but
that the end of the tube, nourished by the embryo-sae, becomes
the future plant.

FERTILIZATION 145

In 1842 Hartig described an “ egg” in the embryo-sac, and
claimed that the pollen-tube carries a substance that fertilizes
the egg, a view which Schleiden promptly opposed. In the
same year Amici reiterated his previous views and claimed for
Orchis and other plants the preexistence in the embryo-sac of
a cell which, through the influence of the pollen-tube, becomes
the embryo. Schacht opposed this claim, and suggested that
such antiquated ideas be abandoned. At the same time, Hugo
von Mohl described the ege-apparatus in Orchis Morio, and
warmly supported Amici’s views.

In his conclusion Schacht says: “ The tendency to error is
so bound up in human nature that the work of one’s mind, like
that of his hand, is never perfect, and consequently I do not
consider my work free from error and misconception, but I have
tried to minimize these as much as possible. In the chief

Fie. 66.—A, Staphylea; tip of pollen-tube showing division of generative nucleus. B,
Orchis latifolia; end of pollen-tube showing tube nucleus (in advance) and the
two male nuclei. C, Monotropa Hypopitys; fusion of sex nuclei, male nucleus
more deeply shaded. D, the same stage just after fertilization, showing first division
of endosperm nucleus, x 450.—After STRASBURGER.®

matter, the origin of the embryo from the pollen-tube, no one
can convince me that there has been any error or misconcep-

146 MORPHOLOGY OF ANGIOSPERMS

tion.” Nevertheless, in his text-book, published a few years
later, he says that “ fertilization” is accomplished in plants,
as in animals, by the union of male and female elements.

It is only since 1875 that detailed information has gradu-
ally accumulated ; and not until 1884 (Strasburger 8) were the
eells concerned in fertilization clearly pointed out (Fig. 66).

The tube-cell of the pollen-grain in various ways pushes
through the exine a papillate protrusion of the intine that
develops into the pollen-tube with greater or less rapidity.
Crowding among the loose papillate cells of the stigma, the
elongating tubes enter the conducting tissue of the style. Ordi-
narily the style is solid, and the tubes grow along the conducting
strand, which they disorganize more or less, obtaining from it
their nutritive supply. In case there is a stylar canal the tubes
either pass down it, as in Pontederia (Smith *5) and Lrythro-
nium (Schafiner **), nourished by the lining glandular, cells,
or they may penetrate the stylar tissue about the tube, as in
Campanula (Barnes *) and Juglans (Nawaschin *°). In many
cases the tube enters the ovary cavity close to the micropyle;
in others it must traverse more or less of the cavity, being
“onided” to the micropyle by various mechanical and nutri-
tive contrivances.

Although ordinarily pollen-tubes are developed only in con-
tact with the stigma, in cleistogamous flowers tubes have been
observed issuing from pollen-grains still in the anther, the tips
being directed toward the stigma. In Asclepias also multi-
tudes of tubes sometimes start from the unremoved pollinia.

The time elapsing between pollination and fertilization, as
inferred from the presence of pollen-tubes in the embryo-sac,
is extremely variable, and seems to hold no relation to the dis-
tance traversed, as shown by Hofmeister,* in comparing Crocus,
in which a style 6 to 10 em. long was traversed in one to three
days, with slrum, in which a style only 2 to 3 mm. long was
traversed in five days. The range in time is probably repre-
sented by the following illustrations: In Limnocharis emargi-
nata Hall®? found a two-celled embryo in material killed
eighteen hours after pollination, and thinks that in this case
fertilization probably oceurs the first night after pollination.
Probably the most aceurate estimate of the time is that by
Mottier *® for Lilium, in which the time between artificial pol-

FERTILIZATION 147

lination and fertilization (as shown by fusion) was sixty-five to
seventy-two hours. Guignard °° has recorded an interval of two
days between pollination and fertilization in Nicotinana Taba-
cum. Juel® found by artificial pollination that fertilization
occurs in Cynomortum four days after pollination, sixteen
days after pollination embryos of various sizes being found.
Hofmeister? noted the interval as one to three days in
Crocus, five days in Arum, from ten days to several months
among the Orchidaceae, and in Colchicum autumnale not less
than six months (November to May). In the last case, as is
well known, pollination sometimes occurs before there is any
appearance of ovules. Miss Benson !° found three weeks elaps-
ing in Fagus sylvatica between pollination and the entrance of
the tube into the embryo-sac, and the same interval is reported
by D’Hubert 17 for certain Cactaceae. In Hamamelis virgini-
ana Shoemaker °° has found that pollination occurs from Octo-
ber to December; that the tubes develop at once and grow
rapidly until cold weather; that during January and February
the tube may be found safely embedded in the hairy part of the
earpel; and that growth is resumed in the spring, fertilization
occurring about the middle of May, five to seven months after
pollination. The pollen-grains of Hamamelis show great resist-
ance to low temperature, Shoemaker citing cases in which they
produced tubes after exposure to a week of cold, the tempera-
ture sometimes being as low as —15° C. Among the Amentif-
erae, however, the interval becomes even more extended. Miss
Benson? reports that it is one month in Betula alba, two
months in Carpinus Betulus, three months in Alnus glutinosa,
four months in Corylus Avellana and Quercus Robur, and as
much as eleven months in certain other oaks; while in Q. velu-
tina Conrad *° found the interval between pollination and fer-
tilization to be thirteen months. Baillon had long before noted
that no indication of ovules is present in Quercus at the time
of pollination. Goebel? has associated these long intervals
with the woody habit, citing Ulmus, Quercus, Fagus, Juglans,
Citrus, Aesculus, Acer, Cornus, and Robinia as illustrations,
and stating that the interval is almost a year in American oaks
that take two years to ripen their seed. Such cases bear a
striking resemblance in this regard to many Gymnosperms.

A recent study of Monotropa uniflora by Shibata ® indi-

148 MORPHOLOGY OF ANGIOSPERMS

cates that the interval between pollination and fertilization in
any given species may be dependent upon temperature. In the
ease of Monotropa, under normal conditions fertilization takes
place about five days after pollination ; but by lowering the tem-
perature the interval is lengthened, and at 8-10° C. fertilization
is prevented. In Shibata’s experiments it was shown that
light, atmospheric pressure, and mechanical injury seem to
exert no influence upon fertilization and subsequent phenomena,
but that the structures of the embryo-sac are very sensitive to
temperature.

Tn a long pollen-tube, or in one that persists for a long time,
it is common to observe the formation of successive cellulose
plugs (Propfen) that shut off the growing tip, with its cells
and nuclei, from the cavity behind, as fully described by Stras-
burger * and Elfving.* Sometimes the plugs are so large and
persist in such a series that they become conspicuous objects,
as in Gymnadenia conopsea (Marshall-Ward?), Campanula
americana (Barnes ®), Sarcodes sanguinea (Oliver ++), ete. In
such forms as the Amentiferae and others, in which the tube
and its contents remain imbedded in the stylar tissue for a
period varying from one month to over a year, the tip of the
tube is cut off by a plug, its wall thickens, and it passes into
what might fairly be called an encysted condition, as suggested
by Miss Benson ?° in connection with Carpinus.

The branching of pollen-tubes, so conspicuous a phenome-
non among Gymnosperms, is also found among certain Angio-
sperms. Hofmeister * observed branching tubes among Mono-
cotyledons in Pothos longifolia and Hippeastrum aulicum.
Among the Amentiferae it seems to be very common, Miss
Benson 1° observing forking tubes in several of the genera
(Corylus, Carpinus, ete.) she studied, and in Quercus a cluster
of short branches at the end of the tube; while Nawaschin 2°: 2°
states that the tubes of Juglans and Ulmus branch protusely,
and recently a similar branching has been noted by Billings ®*
in Carya (ficoria). Zinger *! also deseribed the pollen-tubes
of the Cannabineae as ending in numerous swollen sae-like
branches. The breaking up of the tip of the tube into short
branches is doubtless a common phenomenon, probably associ-
ated with the rhizoidal habit, but free branching seems to be
characteristic chiefly of chalazogamie forms. :

FERTILIZATION 149

In 1891 Treub 1° announced the phenomenon of chalazog-
amy in Casuarina. He found the pollen-tube penetrating the
chalazal region of the ovule, instead of entering through the
micropyle. In this case the pollen-tube becomes associated with.
the numerous elongated sterile megaspores, and doubtless they
are of service in rendering the passage easy; and later it enters
the antipodal region of the embryo-sac and approaches the egg-
apparatus from that direction (Figs. 67, 240). In 1893
Nawaschin’* reported chalazogamy in Betula; and in 1894
Miss Benson ?° not only observed the phenomenon in Betula,
but also added Alnus, Corylus, and Carpinus to the list of
chalazogamic plants. In all of these cases Miss Benson ob-
served the tubes following a course
parallel with the vascular strands
of the raphe, thus reaching and \\
penetrating the chalaza. In Cory-
lus and Carpinus the tube enters
a more or less conspicuous caecum
developed in the antipodal region
of the sac, traverses it, and comes
in contact with the egg; but in
Alnus the tube traverses the nucel- A
lus to the micropylar region above
the -embryo-sac, and then tine, Oe re re

: pollen-tube entering chalazal end
and enters it as though it had come of embryo-sac, x 270; B, stage
by way of the micropyle. In 1895 showing (Treub’s interpretation)
Nawaschin *° added Juglans cine- aa ae Peseta

ilization, x 180. After TREvs.

rea and J. regia to the list. In the

latter species the tube does not pass down the stylar canal or
traverse the cavity of the ovary, but advances through the tissue
of the style and of the ovary wall until opposite the insertion of
the single ovule that fills the ovary cavity. It then leaves the
ovary wall and pierces the chalaza, branching freely in the nu-
cellus, which is described as “ veined ” by tubes surrounding the
sac on all sides. The male nuclei discharged into the sac were
seen “ wandering ” in its cytoplasm and fusing with one of sey-
eral free cells that function as eggs but have not organized an ege-
apparatus. Recently Billings °° has discovered chalazogamy in
Carya olivaeformis, the common pecan, the details conforming
almost exactly to those given by Nawaschin for Juglans regia.

150 MORPHOLOGY OF ANGIOSPERMS

Tn 1898 Nawaschin ®° described some remarkable variations
in the course of the pollen-tube in Ulmus pedunculata and U.
montana. In addition to tubes following the ordinary chala-
zoganie route, some instead of penetrating the chalaza pass
from the funiculus across the short outer integument, and
thence into and upward through the inner integument to the
top of the nucellus, when they turn across to the bottom of the
micropyle and so enter the nucellus from the usual direction ;
others follow the same route except that they pass directly from
the funiculus into the inner integument; while still other tubes
branch profusely and apparently with no definiteness within
both the funiculus and integument. In the same species, there-
fore, pollen-tubes may enter the sac either at the antipodal or
micropylar ends, and may either pass with great directness or
branch profusely.

The behavior of the pollen-tubes in U/mus suggested that
there might be other routes than through the micropyle or
through the chalaza, and this has been observed in other forms.
In his study of the Cannabineae in 1898, Zinger *! discovered
that the two thick integuments completely coalesce over the
apex of the nucellus, and the micropyle is entirely closed by
tissue. The pollen-tube either bores its way through the tissue
fillmg the micropyle or pierces the two integuments, reaching
the nucellus and branching about its apex, and finally sending
one very slender branch into the embryo-sae.

With these facts before them, Pirotta and Longo *! pro-
posed the term “ acrogamy ” for the entrance of the pollen-tube
directly through the micropyle; “ basigamy ” for its entrance
through the chalaza (Casuarina, Betula, Alnus, Corylus, Carpt-
nus, Juglans, and sometimes U7mus): and * mesogainy ” for
its entrance by intermediate rontes (sometimes Ulmus, and
Cannabineae). In the following year Longo *° described a ease
of mesogamy in Cucurbita, in which the pollen-tube traverses
the tissues of the funiculus and outer integument before enter-
ing the micropvle. Practically the same phenomenon has been
observed by Murbeck °° in Alchemilla arvensis, in which the
micropyle is entirely closed by the growth of the integument,
and the pollen-tube enters the ovule at the chalazal end, trav-
erses the entire length of the integument within its tissues, and
thus enters the micropylar extremity of the embryo-sae.

FERTILIZATION 151

True chalazogamy, therefore, has as yet been found only
among the Amentiferae, but such an intermediate condition
as shown by Ulmus, Cucurbita, and Alchemilla, in which the
pollen-tube enters the ovule at the chalazal end, but traverses
the integument instead of the nucellus, suggests that chala-
zogamy is an exceptional condition derived from the ordinary
route of the pollen-tube through the micropyle. In certain
sases the tube reaches the micropyle by passing along more or
less of the surface of the integument; in other cases it enters
the tissues of the integument, and finally it penetrates deeper,
entering the chalazal tissue. This seems to be a natural
sequence of events that resulted in chalazogamy, which there-
fore would hold no relation to a primitive condition of Angio-
sperms or to their classification.

In passing through the micropyle the pollen-tube is more
or less compressed, and upon reaching the wall of the embryo-
sac may broaden out upon it. In some cases (p. 94) the
synergids have already pierced the wall of the embryo-sac, but
in most cases it must be pierced by the tube. Upon entering the
sac the tube either passes between the synergids, as in Ponte-
deria (Smith ?), Muphorbia (Lyon **), sometimes Salix
(Chamberlain **), ete. (Fig. 44); or between the sac-wall and
one synergid, as in Alisma (Schaftnér **), Liliwm (Coulter **),
Ranunculus (Coulter *7), Magus (Benson '*), Silphium (Mer-
rell*°), ete. Recently, however, Guignard °° has reported that
in Nicotiana Tabacum and Datura laevis the tube passes into
a synergid and discharges its contents into the broken-up body.
So far as our own observation goes, the usual route of the tube
is between the sac-wall and one of the synergids, but this may
well vary even in the same species. Within the sac the tip
of the tube usually becomes much swollen, often appearing
pouch-like, as in Alisma, Erythronium, Ranunculus, Silphium,
etc., due probably to the rapid absorption of material from the
synergid. As a rule, one synergid is disorganized by its contact
with the tube; but in Salix (Chamberlain **) (Fig. 44), Szl-
phium (Merrell *°), Nigella (Guignard **), etc., cases of fer-
tilization have been observed in which both synergids remained
intact; while in Hrigeron (Land **) both synergids are fre-
quently disorganized. D’Hubert** has made the interesting
observation in connection with his study of the Cactaceae that

11

152 MORPHOLOGY OF ANGIOSPERMS

the nucleus of one synergid moves toward the tube upon its
entrance into the sac, ‘and that the nucleus of the other synergid
moves toward the nucleus of the egg.

In case the tube passes between the synergids
directly toward the egg-nucleus; but in case it passes along the
wall of the sac the tip of the tube curves toward the eve-nucleus.
In any event, the tip of the tube, in which a thin area (pit)
is developed, is directed toward
the ege-nucleus when the dis-
charge takes place. Under the
pressure developed by the turgor
of the end of the tube, and re-
sisted by the small caliber of the
tube in its passage through the
micropyle and sac-wall, the

it advances

membrane of the pit is ruptured,
and a discharge of the contents
results. The perforated tip of the
pollen-tube, after the discharge,
has been demonstrated — fre-
quently, as seen by Schaffner **
Fie. 68.—Sagittaria variabilis. Pollen- in Sagittaria (Fig. 68). The
tube in the act of discharging; four discharge seems to be forcible
centrosomes represented; x 900— : ai i rep
ake eee ae enough to empty the end of the
tube of most of its contents, the
most important ones being the two male nuclei. Cases have been
reported in which only one male nucleus is said to be discharged,
as in Alisma (Schaffner 7?) and Sagittaria (Schattner **), the
other being recognized as degenerating in the tube. However,
the frequent presence of disorganizing bodies within the tube
after fertilization (Fig. 71), and numerous observations of the
discharge of both male nuclei, and especially the rapidly multi-
plying illustrations of ‘* double fertilization,” incline to the be-
het that the discharge of both male nuclei into the sae is usual.
The passage of the male nucleus through the eytoplasm of
the egg toward the female nucleus may be attended by an
increase in size and change in form, but the changes are not 30
conspicuous as those that occur in the male nucleus that passes
deeper into the sae to fuse with the polar nuclei. For example,
in Caltha palustris Miss Thomas ** found the male nuclei very

FERTILIZATION 153

small and oblong or lenticular on extrusion, the one passing to
the polar nuclei increasing very much in size, the other very
little. In Tricyrtis hirta Ikeda ** found the male nucleus that
passes to the polar nuclei showing ‘‘ enormous change in size
and shape” as it passes through the sac. There is usually more
or less elongation of male nuclei at the time of discharge or
afterward, but in Monotropa uniflora Shibata °* has seen them
elongated when entering the sac, but becoming more nearly
spherical as fusion progresses. In the pollen-grain at the time
of shedding the generative nucleus stains blue and the tube
nucleus red with a combination lke cyanin and erythrosin.
This reaction is maintained, the male nucleus staining blue
even after coming into contact with the nucleus of the egg
which stains red; but as fusion proceeds the male nucleus takes
less and less of the cyanin and finally stains with erythrosin
like the nucleus of the egg.

The fusion of the male and female nuclei may be very
rapid, as observed by Guignard ** ** in Zea and Ranuncula-
ceae; or the two may be long in contact without fusion, as noted
by Johnson ** in Peperomia. The behavior of the chromatin
during fusion has received but little attention. Mottier °° fig-
ures the chromatin when the nuclei are partly fused, and the
statement is generally current that the nuclei fuse in the resting
condition (Fig. 69). In view of
the independence of the pater-
nal and maternal chromatin dur-
ing fertilization in Gymno-
sperms, as recently noted by
several investigators, it would be
well to reexamine the subject in
Angiosperms, especially since
most observers have paid little
or no attention to this phase of
the problem. une

Since it has been in connec- Fie. 69.—Lilium candidum. Fusion of
tion with fertilization and at- sex nuclei; the synergids appear as
tendant phenomena that the cen- sat Deva ay maseee A Mer

. MOTTIER.
trosome problem has come into
greatest prominence, it may not be inappropriate to refer to the
subject at this point. Guignard, Schaffner, and others have

154 MORPHOLOGY OF ANGIOSPERMS

regarded the centrosome as a permanent organ performing an
important function in mitosis and in fertilization. Even the
“quadrille of the centers,” described by the zoologist Fol, was
identified by these observers. Centrosomes in the vascular
plants have been figured by many other prominent botanists,
including Humphrey,'® Strasburger,!® Campbell,® and Mot-

PA ny
it

‘yl it

Fie. 70.—Figures of centrosomes in vascular plants. 4, Zilinm Martagon, the reduction

division at germination of megaspore ; 12 chromosomes may be counted: x 600:
ha eee " ee » Pe el as . ‘ : : ;
after GuienarpJ§ By Larix europaea, first division ot pollen mother-cell

: x 600;
after SrrasBURGERIS — C! Delphinium tricorne, tirst a

ivision of megaspore mother-
cell; “at upper pole are centrospheres”: x 588: after Mortier.! 2), Sagittaria
variabilis, first division of pollen mother-cell; x 640 > after SCHAFFNER.24 E Tilscin
eandidum, reduction division at germination of megaspore ; after Buewand.? F,
Psilotum triquetrum, first division of spore motl '

Soy rer-cell ; x 800; after Humpurey.'9
G, Lquisetum telemateia, tetrad of tour spores ;

x 9605 after CAMPBELL.!®

ae ae ee re : : :
tier “° (Hig. 70). Most botanists, following Strasburger, have
yublicly renounced any belief i centros san 5
I \ ounced any belief in the centrosome as an organ of

FERTILIZATION 155

vascular plants, and many others have made a tacit renuncia-
tion. To say that all the figures that have been drawn have

Fie. 71.—Double fertilization. 4, Helianthus annuus, showing the two coiled male

nuclei, one fusing with the egg-nucleus and the other with the endosperm nucleus;
after Nawasonin.49 B, /ris, the two polar nuclei not yet fused; after Guienarp.3?
C, Silphium laciniatum : sp,, sp2, male nuclei; 0, oosphere; e, endosperm nucleus;
sy, synergid; pt, pollen-tube; x, two conjectural bodies often seen in the pollen-
tube after the male nuclei have been discharged ; x 525; after Lanp.38

been mere products of the imagination would be a radical state-
ment, and one doubtless very far from the truth. In our
opinion the observations, figures, and descriptions, like the
pollen-tube embryos of Schleiden and Schacht, furnish an exam-
ple of the extent to which even a careful and conscientious
scientist may be influenced by preconceived opinion.

Our knowledge of the phenomenon called “ double fertili-
zation” (Fig. 71) dates from 1898, when Nawaschin ** ** an-

156 MORPHOLOGY OF ANGIOSPERMS

nounced at a meeting of the Russian Society of Naturalists in
August that it occurs in Lilium Martagon and Fritillaria ten-
ella. In 1899 Guignard ** observed the same phenomenon in
Lilium pyrenaicum, Fritillaria meleagris, and = Hndymion
nutans. During 1900 the literature of the subject increased
rapidly. Nawaschin *? added Juglans, Delphinium elatum,
Rudbeckia speciosa, and Helianthus annuus to the list, and in
certain orchids (Arundina and Phajus) he found the second
male nucleus consorting with the polar nuclei, but there was no
fusion. Guignard ** described the phenomenon in species of
Tulipa (Fig. 72), also *? in Seilla, Narcissus, Reseda, and
Hibiscus; and Strasburger ** not only added Himantoglossum,

es : : : ‘ :

Fic. 72.—A, embryo-sac of Tulipa sylvestris, showing nuclei scattered irregularly, each
nucleus surrounded by a rather definitely limited portion of the cytoplasm; x 300.
B, T. Celsiana, showing double fertilization in sac like that shown in A; the male
nuclei recognized by vermiform appearance; x 333.—After Gurenarp.s?

certain species of Orchis, and Monotropa Hypopitys, but dis-
cussed the whole subject. Miss Thomas‘: #° reported double
fertilization in Caltha palustris; Guignard *? announced it in
Ranunculus Flammula, Helleborus foetidus, Anemone nemo-
rosa, Clematis, Viticella, and Nigella sativa, and independently
confirmed its oceurrence in Caltha palustris. Tand *8 found it
in species of Hrigeron and Silphium; it was observed repeatedly

FERTILIZATION 157

in this laboratory in Lilium philadelphicum (Fig. 36, H), L.
trigrinum, and Anemone patens Nuttalliana; and at the close
of 1900 Miss Sargant *° published a résumé and general discus-
sion ot the subject. More recently, Guignard * has described
dlouble fertilization in Zea and Naias major; Land has discoy-
ered it in Cnicus and possibly in Taraxacum; while Guignard **
has added Nigella damascena and Ranunculus Cymbalaria ;
and Frye °° has described its occurrence in Asclepias Cornutt.
Karsten °° has also confirmed the occurrence of double fertili-
zation in Juglans, investigating several species; Shibata °* has
added Monotropa uniflora, Ikeda ®* Tricyrtis hirta, Strasbur-
ger °? Ceratophyllum demersum, Guignard °° species of Nico-
tiana and Datura, as well as of Capsella and Lepidium,**
Wylie °* Blodea, and Frye 8 Casuarina.

It will be seen that the phenomenon is not restricted to a
few groups, but is widely displayed among both Monocotyledons
and Dicotyledons; among the former having been observed in
Naiadaceae, Hydrocharitaceae, Gramineae, Liliaceae, Amaryl-
lidaceae, and Orchidaceae; and among the latter in Juglanda-
ceae, Ceratophyllaceae, Ranunculaceae, Cruciferae, Resedaceae,
Malvaceae, Ericaceae, Asclepiadaceae, Solanaceae, and Com-
positae. Probably it is not safe to infer the general occurrence
of double fertilization, although the observations already include
sixteen families, about forty genera, and over sixty species,
besides inferential testimony in other species from the form and
activity of both male nuclei and from the phenomenon of xenia.
In any event, it is common enough to demand a general explana-
tion of its significance, its place in the history of Angiosperms,
and especially whether it is really fertilization or merely triple
fusion. It has certainly introduced among structures already
dificult of interpretation a phenomenon that immensely in-
creases the difficulty. The subject will be discussed briefly
under endosperm (Chapter VIIT), and only such general
details presented here as have been observed in connection with
the process.

It is claimed by Guignard for Liliwm, and confirmed by
Miss Thomas in Caltha, that the first male nucleus extruded
from the tube passes to the polar nuclei. The frequently vermi-
form and spiral character of this nucleus has suggested the possi-
bility of independent motion ; but this form is by no means con-

158 MORPHOLOGY OF ANGIOSPERMS

stant, and Strasburger,*? in examining the process in living
material of Monotropa, demonstrated the passage of the male
nucleus in the streaming protoplasm of one of the cytoplasmic
strands connecting the primary endosperm nucleus or the polar
nuclei with the egg-apparatus. This is confirmed by Guig-
nard,®® who has deseribed and figured the very small male
nucleus passing down the broad cytoplasmic strand that con-
nects the egg-apparatus with the antipodals and envelops the
primary endosperm nuclens in Nigella, Damascena, Ranunculus
Cymbalaria, and Anemone nemorosa, and which is doubtless
true of the other Ranunculaceae. It seems probable that the
male nucleus is generally carried along one of these strands; but
it is not improbable that the vermiform nuclei occasionally
acquire some power of independent motion. It is during this
passage that the male nucleus may increase much in size
(Thomas,** Ikeda °*) and may even assume the vermiform
character; although all such changes may have occurred before
discharge from the pollen-tube, even in the pollen-grain, as
observed by Merrell *° in Silphium. The male nucleus, how-
ever, may retain its small size and oval form even in contact
with the polar nuclei, as observed by Guignard *? in Endymion,
and by other observers since. In Juglans Karsten *° believes
that in all cases the polars are fertilized before the egg; but in
Nicotiana Tabacum Guignard °° reports that sometimes the egg
is fertilized first and sometimes the polars, so that probably
there is no definite order in the two fusions.

Every possible order in the fusion of the three nuclei has
been observed, so that the triple fusion is brought about in a
variety of ways. As might be expected, it is often the ease that
the polar nuclei have already fused when the pollen-tube enters
the embryo-sac, and the male nucleus unites with the fusion
nucleus, as in Tricyrtis, Ranunenlaceae, Datura, Brigeron, Sil-
phium, ete.; although even in this case the polar nuclei may not
always lose their individuality. The two polar nuclei and the
male nucleus have also been observed to fuse all together, as in
Zea (Guignard #8) and other plants, in which the vermiform
male nucleus seems to bind the polar nuclei together. In Nicoti-
ana (Guignard *°) the male nucleus comes in contact with either
polar nucleus or both. In Lilium Martagon the male nucleus
usually fuses first with the upper polar nucleus, and later the

FERTILIZATION 159

lower polar nucleus enters the combination, as was also observed
by Shibata ** in Monotropa uniflora; but in Lilium it has been
observed that if the lower polar nucleus happens to be the more
favorably placed the male nucleus fuses with it first. In Ascle-
pias Cornutt (Frye ®°) both male nuclei are vermiform and
more or less curved, and one of them was observed in contact
with a polar nucleus near the antipodal cells, the micropylar
polar nucleus being some distance away and nearer the ege-
apparatus. That the male nucleus may thus traverse much of
the embryo-sac is also shown in Nigella damascena and Anem-
one nemorosa, in both of which Guignard ** observed the male
nucleus uniting with the fusion nucleus near the prominent
antipodal cells.

At present there is a decided tendency among botanists and
zoologists to distinguish two distinct phenomena in fertiliza-
tion—namely, the stimulus to growth and the mingling of ances-
tral qualities. Strasburger ** regards the latter process as the
essential one, and the stimulus to growth as only providing the
conditions which make it possible to obtain the advantages
resulting from a mingling of ancestral plasma masses. In a
later paper °® he makes the statement that fluctuating variations
do not furnish a starting-point for the formation of new species,
but that it is the principal function of fertilization, through
the mingling of ancestral plasma masses, to keep the species
characters constant. The essence of fertilization lies in the
union of organized elements. It was to insure this essentially
generative fertilization that, in the course of phylogenetic devel-
opment, the inability of the sexual cells to develop independ-
ently became more and more marked. The term generative
fertilization is used in contrast with vegetative fertilization,
which is merely a stimulus to growth. Hence Strasburger re-
gards the fusion of the male nucleus with the polar nuclei as
merely vegetative fertilization, and lacking the essential feature
of a sexual fusion. It is worthy of note that Ernst ® finds in
Paris quadrifolia and Trillium grandiflorum a striking differ-
ence between generative and vegetative fertilization, the fusion
of the male nucleus with the egg-nucleus being complete, so
that a typical resting nucleus is formed; while the polar nuclei
begin to form spirems even before the male nucleus arrives, and
in the group of three nuclei—the two polar nuclei and the male

160 MORPHOLOGY OF ANGIOSPERMS

nucleus—three spirems are distinguishable, a case observed also
in this laboratory by Miss Laetitia Snow in Lilium philadel-
phicum. In such cases it is very probable that there is no union
of the chromatin (Fig. 73), and it is known that in Pinus there
is no fusion of the chromatin of the two sex nuclei betore the

Fie. 73.—Paris quadrifolia. A, two polar nuclei in spirem stage; male nucleus (m)
shown just above; B, the two nuclei and male nucleus in spirem stage; x 1250.—
After Ernsr.61

binucleate stage of the proembryo is reached, and the majority
of published figures show this condition. However, Land **
describes a complete fusion of the polar nuclei of Si/phiwin
before the union with the second male nucleus.

On the whole, it is to be regretted that the phrase “ double
fertilization ” has been applied to this phenomenon, since it 1s
far from established that it is to be regarded as real fertiliza-
tion. During this uncertainty it would seem convenient and
suflicient to speak of it as “ triple fusion.” Tt is also mislead-
ing to speak of the vermiform male nuclei as * antherozoids ”
or “ spermatozoids ” in the sense that they are something mor-
phologically distinet from the other male nuclei of Angiosperms.
Whatever the ordinary male nuelei of Angiospermggmay be these
vermiform nuclei are. Probably male cells are Werays organ-
ized, and we consider them as morphologically sperm mother-
cells; but it is also probable that only the male nuclei become

FERTILIZATION 161

vermiform and take part in fusion. In preparations of Lilium
we have seen a vermiform nucleus still enclosed by the cyto-
plasm of the male cell. It would be strange morphology to base
the definition of a sperm-cell upon its form or power of inde-
pendent motion.

~t

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162 MORPHOLOGY OF ANGIOSPERMS

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FERTILIZATION 163

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lished in Bot. Gazette 35: 1903.

Tue endosperm

so clear. The ger-
mination of the
megaspore begins,
as in Gymnosperms,
with free and simul-
taneous nuclear di-

vision. In Gymno-

sperms this con-
tinues for some
time and is_ re-

placed by cell-for-
mation, giving rise
to an extensive tis-
sue bearing arche-
gonia, while in An-
giosperms usually
only eight free nu-
clei are formed be-
fore an egg is organ-
ized and fertiliza-
tion takes place. In
both cases — endo-

sperm is formed

after fertilization; but in Gymnosperms it is a continuation
of cell division, while in Angiosperms it usually begins with
nuclear fusion followed by simultaneous and often free nuclear

CHAPTER VIII

THE ENDOSPERM

of Gymnosperms seems to be clearly the
vegetative tissue of the female gametophyte, but the morpho-
logical nature of the endosperm of Angiosperms (Fig. 74) is not

Fie. 74.—Two modes of initiating the formation of endo-
sperm. 4, Vaias major, illustrating free nuclear divi-
sion ; there are four free nuclei belonging to the endo-
sperm, the lower free nucleus being that of the upper

B, Datura laevis, nuclear division

followed immediately by formation of wall ; g

antipodal; x 175.

After GuIGNARD.42, 48

166 MORPHOLOGY OF ANGIOSPERMS

division. This nuclear fusion is one of the most striking fea-
tures of the Angiosperms as contrasted with Gymnosperms, and
especially since the discovery of so-called “ double-tertilization ”
the morphological character of the endosperm of Angiosperms
is in question. For this reason, we have preferred to discuss
it apart from the gametophytie structures concerning which
there is no question.

As has been said, the endosperm of Angiosperms is usually
derived from a fusion nucleus, the constituent members being
the micropylar polar nucleus, sister to the egg, and the antipo-
dal polar nucleus. If the current homologies are true, this
fusion is that of a female and a vegetative nucleus. In many
‘ases a male nucleus also joins in the structure of the primary
endosperm nucleus, which is then the result of a triple fusion
(Pigs. 36, H, and 71-73). How far this male nucleus is an es-
sential factor in the formation of the endosperm of Angiosperms
is at present unknown, but the rapidly increasing number of
plants in which triple fusion has been observed leads to the
belief that it may be of general occurrence. It should also be
remembered that in Peperomia pellucida (Johnson *!) (Fig.
35) the primary endosperm nucleus is the result of the fusion
of no less than eight of the sixteen free nuclei of the embryo-
sac; and that in Gunnera (Schnege ) (Fig. 39) the same sort
of multiple fusion oceurs. The fusion-nucleus, therefore, may
be made up of a variable number of constituents of various
morphological character, and hence the significance of the
fusion and the nature of the resulting tissue are peculiarly dith-
cult to interpret.

While the fusion of these nuclei seems to result in what has
been called a growth-stimulus, endosperm is sometimes formed
without any antecedent fusion. For example, in Balanophora
(Treub,'® Lotsy 2°) the polar nuclei do not fuse, but divide
independently, the embryo-sae becoming filled with endosperm
tissue; and in Helosis (Chodat and Bernard ®*) after the first
division of the nucleus of the megaspore the chalazal nucleus
disintegrates so that antipodal cells, and henee an antipodal
polar nucleus, are not formed, the endosperm being derived en-
tirely from the mieropylar polar nuclens. In Antennaria alpi-
na duel 7% found that the polar nuclei do not fuse, although they
behave normally in A. dioica, as the same investigator 83 has

THE ENDOSPERM 167

observed. In Lemna Caldwell ** states that often the polar
nuclei do not fuse, in which case he observed that the micro-
pylar polar produced some free endosperm nuclei, and probably
the antipodal one also. In Limnocharis, one of the Alismaceae,
there is also no fusion (Hall *°), since no antipodal polar nucleus
is formed, and all the endosperm, which eventually fills the sac,
is derived from the micropylar polar
nucleus. In Casuarina, according
to Treub,!* there are no antipodals
or polar nuclei, and the endosperm
is formed before fertilization and
independently of any fusion (Fig.
67, B). It should be stated, how-
ever, that in a recent study of Casu-
arinad by Frye *? abundant endo-
sperm was found before the first
division of the egg, but probably
not before fertilization. For exam-
ple, the same investigator °° found
in Asclepias sixteen and thirty-two
endosperm nuclei before the first
division of the egg, but not before
fertilization (Fig. 75). In Pauper
and Heckeria the development of
endosperm before the first division
of the fertilized egg is even more
extensive. Johnson ®® represents
twenty-two endosperm cells in a
single section of Piper (Fig. 76)
and the egg has not yet divided.

Fie. 75,—Aselepias Cornuti. Large
x s : development of endosperm before
Not a little confusion has arisen division of fertilized egg: a, an-

by assuming that fertilization and tipodals; ¢, egg; s, synergids; x

Z 1 pare 750.—After Frye.
the first division of the egg are

practically simultaneous. In any event, the formation of endo-
sperm without antecedent fusion is clear enough in some cases,
and indicates that while fusion usually serves to stimulate
growth and cell division it is not an absolute prerequisite. In
certain orchids Nawaschin *° states that the polar nuclei do not
fuse, but in this case no endosperm is formed.

In this connection the experiments of Shibata *? on Mono-

12

Fia. 76.— <A, Piper medium, showing extensive development of endosperm before first
division of fertilized egg; x 175; BUD, Peperomia pellucida: B, longitudinal section
of ripe seed, showing the small embryo, scanty endosperm, and abundant perisperm ;
x 55; C, terminal portion of a similar section at an early stage of germination;

« 175; D, longitudinal section of a germinating seed, showing the endosperm pro-

truding with the embryo; x 55: a, antipodals; ¢, cotyledons; ep, carpellary tissue 5

ce, endosperm ; em, embryo; 7, integument; 0, oosphere ; ~, perisperm ; 7, rhizoid

synergid ; st, stigma; ¢, tapetal cells.—After Jounson.56

168

> 4;

THE ENDOSPERM 169

tropa uniflora are of interest. Jn this case the polar nuclei may
fuse in the absence of pollination, but the fusion may be hastened
or regulated by pollination. In normal cases fusion of polar
nuclei occurs about five days after pollination, but when pollina-
tion is prevented the interval may be prolonged to ten days or
even longer. Development of the endosperm was also induced
experimentally in the absence of fertilization. When pollination
is prevented, many of the ovules die within two or three weeks,
but in others the sac enlarges and becomes filled with endosperm.
This development of en-
dosperm was observed in
from three to five per cent
of the ovules, but at a tem-
perature of 28° C., or by
using osmotic solutions, en-
dosperm was developed by
from six to twelve per cent
of the seeds.

If a fusion nucleus is
formed, as is certainly gen-
erally the case, it usually
begins to divide before the
fertilized egg and with
much greater rapidity.
After fertilization, the egg
usually seems to rest for a

period while free endo-
ie lei z hens Fic. 77.—Evigeron philadelphicus. Longitudinal
BPSD ere: «tie ss sections of embryo-sac after fertilization. 4,

formed. For example, fertilized egg dividing before primary endo-
among the Ranunculaceae — sperm nucleus; B, primary endosperm nu-
(Guienard 43) scat Ae ee eas 3 before egg; x 550.— After
z AND.

clepias (Frye**) free en-

dosperm nuclei are scattered through the sac before the egg
divides. But there is every gradation from an approximately
simultaneous division of primary endosperm nucleus and fer-
tilized ege, as usually in Sagittaria (Schaffner **), Lilium
(Coulter 1°), Nelumbo (Lyon **), Sarcodes (Oliver 11), Senecio
(Mottier 1°), and Erigeron (Land **) (Fig. 77), in which last
case sometimes the egg and sometimes the primary endosperm
nucleus divides first, to a sac almost or even completely filled with

170 MORPHOLOGY OF ANGIOSPERMS

endosperm before the fertilized egg segments, as in CGonyanthes
candida (Treub"), Hechkeria (Johnson *’), the Stylidaceae
(Burns **), and Aphyllon uniflorum (Smith *"). Even though
the primary endosperm nucleus and the fertilized ege divide
simultaneously, the much more rapid divisions of the former
result in numerous free endosperm nuclei before the first few
seginentations of the egg have been completed.

In the eases just cited, in which the segmentation of the
primary endosperm nucleus precedes that of the fertilized egg,
the division does not begin until after fertilization, and proba-
bly this is true in the majority of plants. As a consequence,
the impression is current that the act of fertilization is an
essential stimulus to the division of the primary endosperm
nucleus; and there seems to be no clear evidence to the contrary
when fertilization occurs, unless it be the ease of Ranunculus,
as reported by Coulter,?° in which free endosperm nuclei were
sometimes observed scattered through the embryo-sae before the
entrance of the pollen-tube. To this same category belong those
cases of habitual failure of fertilization in which endosperm
formation may occur, as in the Balanophoraceae, Antennaria
alpina (Juel**), Thalictrum purpurascens (Overton ®!), Bich-
hornia crassipes (Smith *"), ete. It seems to be very rare for
the fertilized egg to divide before the primary endosperm nu-
cleus, but in Natas major, in which triple fusion oceurs, Guig-
nard *” has observed that the fertilized egg divides immediately,
and has figured a two-celled embryo by the side of a primary
endosperm nucleus in the spirem stage. It is important to
note also that in this same species Guignard observed that the
male nucleus may fuse with the persistent synergid instead of
with the primary endosperm nucleus, in which case there is no
endosperm, but a second embryo (Fig. 103). Many eases of two
embryos lying side by side with an “ unfertilized” primary

endosperm nucleus between them were observed. Reeently
Wylie ®° has observed that in Hlodea also the fertilized eee

divides before the primary endosperm nucleus.

It is evident that the beginning of endosperm formation
does not depend absolutely upon any of the causes usually
assigned ; and that while it is in general approxunately coinci-
dent with the segmentation of the fertilized ege, this is merely

a coincidence, for it may be independent of fertilization and

THE ENDOSPERM 171

even of fusion. Ordinarily it must be dependent upon polar
fusion, and in some cases upon triple fusion, as indicated by
the behavior in Naias cited above; but in the failure of these,
other conditions may cause nuclear division and the formation
of endosperm.

While in the majority of plants the endosperm may be re-
garded as fully developed, either to remain as a permanent
tissue of the seed or to be more or less resorbed by the growing
embryo, there are certain plants in which it is abortive or even
suppressed. It consists of only a few scattered nuclei, or at
most of a parietal layer of free nuclei, in Naiadaceae, most Alis-
maceae, Juncagineae, and Iydrocharitaceae, all of which belong
to the Helobiales among Monocotyledons. The tendency of the
endosperm to become abortive in this particular alliance is evi-
dently very strong, although, as Hall °°? has shown in Limno-
charts, the endosperm may finally develop and become packed
about the embryo. With the exception of the Helobiales, disap-
pearance of the endosperm seems to be very rare, having been
reported in T'ropaeolum and Trapa; and among the Orchida-
ceae the endosperm seems to be entirely suppressed, the polar
nuclei, as a rule, neither fusing nor dividing.

Humphrey ** has called attention to what he calls a pro-
gressive series in the development of the endosperm among the
Scitamineae, but which seems to be best interpreted as a retro-
gressive series. In the Musaceae an abundant starch-bearing
endosperm either fills the sac (Heliconia) or nearly so (Stre-
litzia), the peripheral cells often forming an aleurone layer;
in Zingiberaceae (Costus) the endosperm is several layers thick
in the lower part of the sac and only aleurone-bearing; in Can-
naceae (C'. indica) the endosperm is a single aleurone-bearing
layer lining the sac; while in Marantaceae (Thalia dealbata)
the endosperm is probably not represented at all in the mature
seed.

Strasburger * has called attention to the two general meth-
ods of endosperm formation among Angiosperms. In the ma-
jority of plants observed it begins with free nuclear division ;
but in many eases, chiefly among Dicotyledons, the first division
otf the primary endosperm nucleus is accompanied by a wall
dividing the sae into two chambers (Fig. 74). While these
two methods of initiating endosperm formation are quite dif-

172 MORPHOLOGY OF ANGIOSPERMS

ferent, the subsequent stages of endosperm development result
in all kinds of intergrading conditions, as will be shown later.
Even when the endosperm begins with free nuclear division,
a rudimentary plate often appears, suggesting derivation from
an endosperm in which nuclear division was followed by cell-
formation.

The history of the development of endosperm initiated by
free nuclear division is nearly identical, in most cases, with
the history of the female gametophyte in Gymnosperms, modi-
fied, of course, by the presence of a developing embryo. It is
an interesting fact, also, that the early stages in the develop-
ment of the endosperm bear a striking resemblance to early
stages in the development of the embryo of Cyeadales and some
other Gymnosperms. There is the same simultaneous nuclear
division, often the parietal placing, and later the appearance of
cell walls.

The primary endosperm nucleus, usually in contact with
the egg, or nearly so, divides, and subsequent divisions follow
with great rapidity, Guignard #1 remarking that in Zea he was
unable to follow the course of division, and other observers eall-
ing attention not only to the great rapidity with which one set
of divisions is followed by another, but also to their simultane-
ous character. A common form of statement is that at first the
free nuclei remain for a time in the vicinity of the egg, but
sooner or later migrate in every direction toward the wall of
the embryo-sac, where they become equally distributed and
embedded in a lining cytoplasmic layer. The real faet, how-
ever, is that this apparent movement of the nuclei is due to the
rapid enlargement of the sae, the evtoplasm becoming more and
more vacuolate and finally occurring chiefly as a wall layer.
By this increasing vacuolation the nuclei are naturally driven
to the wall. In this parietal position free nuclear division con-
tinnes, until finally walls are formed and a laver of parietal
cells is organized.

These first walls usually “eut out” only one nucleus in
each cell, but in some eases (Corydalis cava, Staphylea pinnata,
Armeria vulgaris, ete.) Strasburger* noted that two to four
nuclei might be enclosed by a cell wall, but that they afterward
fuse to form a single nucleus (Fig. 78). Tischler 39 has
recently reexamined Corydalis cava and states that when septa

THE ENDOSPERM 1738

appear many nuclei are always enclosed in each cell and sub-
sequently fuse. In this particular case the free nuclear divi-
sions are often irregular, and of course the number of chromo-
somes is exceedingly variable, a fact very common in all endo-

Fic. 78.—Advanced stages in development of endosperm. A, Reseda odorata, upper
part of figure showing free nuclear division, while in lower part nuclear division is
accompanied by formation of cell walls; x 860; B, Caltha palustris, showing all
nuclear divisions accompanied by formation of walls, x 155; C, Corydalis cava,
showing free nuclear division within cells of endosperm; D, the same, showing
multinucleate endosperm; x 860.—After SrRasBURGER.*

sperm. The same phenomenon was observed by Humphrey uy
in Canna indica, in which the parietal layer of free nuclei
becomes blocked out by walls, each “ block ” containing several

174 MORPHOLOGY OF ANGIOSPERMS

nuclei that apparently fuse into one. The irregular and usu-
ally large nwmber of chromosomes found in the nuclei of endo-
sperm tissue is doubtless due to “ double fertilization” and
other nuclear fusions.

The parietal plate of cells by division gradually encroaches
upon the general cavity of the embryo-sac, either filling it up
compactly about the embryo, or leaving more or less of a cavity
containing cell sap, which in the coconut becomes of extraordi-
nary size.

In many cases a fully developed endosperm is more or less
displaced by the growing embryo, so that in the mature seed it
may be much reduced or even obliterated. Among the Mono-
cotyledons the embryo of the Gramineae is at first completely
invested by endosperm, but becomes eccentric by displacing it
on one side; and the embryo in some Araceae finally replaces
all the endosperm; but for the most part the Monocotyledons
are characterized by retaining the endosperm in the mature
seed. Among the Dicotyledons, however, it is characteristic of
certain families, among the important ones being Cupuliferae,
Leguminosae, Cucurbitaceae, and Compositae, for the embryo
to have entirely displaced the endosperm at the maturity of the
seed, the gain in size being almost entirely in the cotyledons.
It must not be supposed that in all cases the formation of endo-
sperm continues from the first free nuclear division to a tissue
filling the embryo-sac. Illustrations could be introduced show-
ing a cessation of endosperm formation at every stage. It may
stop with a few free nuelei, or with the parietal placing of free
nuclei, or with a parietal plate of tissue. An interesting ease
is that of Tricyrtis (Liliaceae), recently deseribed by Ikeda,
in which free endosperm nuclei are distributed through a sae
full of eytoplasm, and assume very irregular and bizarre forms,
the parietal position never being assumed.

The second general method of endosperm formation—
namely, that in which the first division of the primary endo-
sperm nucleus is accompanied by a wall dividing the sae into
two chambers—is found chiefly among Dicotvledons, and among
them it is especially characteristic of saprophytic and parasitic
forms, Cuscuta being a marked exception in that its endosperm
begins with free nuclear division. Usually the wall divides the
sac into two approximately equal chambers, but naturally the

THE ENDOSPERM 175

relative size of the chambers depends upon the position of the
dividing nucleus (Fig. 74).

Among Monocotyledons, the endosperm of Sagittaria
(Schaffner '*) develops rapidly in the micropylar chamber
into a walled tissue, the endosperm nucleus of the antipodal
chamber enlarging much but not dividing for a long time, when
two or three nuclei may be formed, all of them increasing
greatly (Fig. 79). Practically the same thing occurs in Limno-
charis (Hall°°), but the nucleus of the antipodal chamber en-
larges without dividing. In Ruppia rostellata (Murbeck °°) a

Fic. 79.—Sagittaria variabilis. A, two nuclei of endosperm separated by wall: a, an-
tipodals, x 200; B, compact endosperm tissue developed from upper cell, the lower
merely growing large without dividing; x 108.—After Scuarrner.’*

wall is formed at the first division of the endosperm nucleus, the
antipodal chamber remaining small and with undividing nucleus,
but a large number of free nuclei being formed in the micro-

176 MORPHOLOGY OF ANGIOSPERMS

pylar chamber. In Potamogeton (Holferty **) the endosperm
is developed only as a parietal layer of free nuclei; but all of
these seem to have come from the micropylar endosperm-cell
of the first division, the lower one becoming very large but not
dividing, a tendency similar to that in Sagittaria and Limno-
charis, but without the formation of a transverse wall in the sac.

Among the Dicotyledons instances of a chambered embryo-
sac are numerous. Hofmeister? has given a long list of them,
and these, with others added since, are approximately as follows:
Among the Archichlamydeae they are the Saururaceae, Loran-
thaceae, Balanophoraceae, Santalaceae, Aristolochiaceae, Nym-
phaeaceae, Ceratophyllaceae, Loasaceae, a list composed in the
main of primitive or saprophytic and parasitic forms. In fact,
the chambered sae is distinctly lacking in the more important
and characteristic groups of the Archichlamydeae. Among the
Sympetalae, chambered sacs occur in the Pyrolaceae, Mono-
tropaceae, Vacciniaceae, Hydrophyllaceae (Nemophila), Sola-
naceae, Verbenaceae, S ‘aginaceae, Labiatae, Scrophulariaceae,
Orobanchaceae, Big s1uceae, Pedaliaceae, Acanthaceae, Plan-
taginaceae, and Campanulaceae. Although most largely repre-
sented among Sympetalae, it will be noted that chambered
sacs occur chiefly in saprophytic or parasitic forms, and among
the Personales. The phenomenon seems thus to be associated
with peculiar conditions of nutrition or a certain configuration
of the embryo-sae.

In the case of two-chambered sacs among Dicotyledons, it
does not seem to be common for endosperm to form in both
chambers, although this is reported to be the case in Balano-
phoraceae, Aristolochiaceae, Pyrolaceae, and Monotropaceae.
In the majority of cases the endosperm develops only in the
micropylar chamber, in connection with the embryo, as in Sau-
ruraceae, Viscwm (Loranthaceae), Santalaceae, Nymphaeaceae,
Globularia (Selaginaceae), Scrophulariaceae, and Orobancha-
ceae. In Saururus (Johnson **) the embryo-sac is flask-shaped,
the wall eutting off the neck from the large venter, and the ev-
dosperin developing only in the former. In Nymphaea and
Nuphar (Cook **) the endosperm develops only in the miero-
pylar chamber, while the antipodal chamber extends as an haus-
torial tube to the chalazal extremity of the ovule. It is of interest
to note that until Cook’s work the endosperm of these genera was

THE ENDOSPERM LTT

said to begin with free nuclear division, followed by a wall cut-
ting off the micropylar end of the sac; and the same statement
in reference to Ceratophyllum has been disproved recently by
Strasburger.*” The endosperm is said to develop only in the
antipodal chamber in Loranthus, Vacciniaceae, Verbenaceae,
Hebenstreitia (Selaginaceae), Bignoniaceae, and Acanthaceae.
In Trapella (Oliver), a genus of the Pedaliaceae, although
the sae is not chambered by a wall, the endosperm develops only
in the lower two-thirds, a sort of diaphragm of thick-walled en-
dosperm-cells cutting off the broad micropylar end of the sae.

Fie. 80.—Ceratophyllum submersum. Development of endosperm and embryo. A, first
division of embryo, six cells in endosperm; x 250; B, embryo and endosperm more
advanced ; x 250; C-D, entire embryo seen from opposite sides, ( showing the two
cotyledons separate and D nearly united; x 50.—After SrraspurGer.‘?

Cases are also known in which more than two chambers are
formed in the embryo-sae and followed by ordinary cell-forma-
tion. For example, in Ceratophyllum (Strasburger *°) at the
first division of the primary endosperm nucleus the sac is
divided into two approximately equal chambers. The nucleus
in the antipodal chamber does not divide again, but at the next
division in the micropylar chamber another wall across the sac

17

[o a)

MORPHOLOGY OF ANGIOSPERMS

is formed, so that there are three superposed chambers, and only
in the one nearest the micropyle does division proceed. As a
result, a dense, small-celled tissue is formed near the embryo
(Fig. 80). In Datura laevis (Guignard **), after the first divi-
sion into two chambers (Fig. 74), transverse walls are formed
in each, resulting in four superposed chambers in which further
division proceeds in various planes.

There are also cases in which each division of an endosperm
nucleus is accompanied by a transverse wall across the sac, as
in Sarcodes (Oliver), in which the mature sac is several-
chambered by a series of delicate transverse walls. The same is
doubtless true of Pistia, whose narrow sae contains a row of
broad discoid endosperm-cells that lie like transverse chambers.
One of the most exceptional cases of wall-formation, however,
is that of Peperomia pellucida (Johnson #1), in which the first
division of the very large primary endosperm nucleus, formed
by the fusion of eight nuclei, is followed by a wall from the
fertilized egg to the base of the sac, further divisions following
until the sac is packed with forty or more endosperm-cells. In
a recent study of Heckeria also, one of the Piperaceae, the
saine investigator °° has found the same general condition as in
Peperomia, in that the endosperm is * cellular’ from the first,
fillmg the sac before the egg divides. It is worthy of note that
the endosperm of Piper (Johnson °°), on the other hand, begins
with free nuclear division. It is evident from these differences
in closely related genera, also noted by Hofmeister ? and Hegel-
maier,® that methods of endosperm formation ean not indicate
relationship.

The mature and permanent endosperm is a tissue with no
intercellular spaces, whose cells are either thin-walled, form-
ing an endosperm of delicate texture, or thick-walled, resulting
ina horny endosperm, as in palms, umbellifers, ete. In ease the
thickening of the walls becomes excessive, the endosperm is
stony, as in Phytelephas, the palm whose seeds furnish the
so-called “ vegetable ivory.”

The endosperm has sometimes been observed to eontinue its
growth after it has filled the sac. Tlofimeister deseribes the en-
dosperm of Crinum capense and some other Amarvllidaceae as
bursting the seed-coats, and even the ovary wall, the cells devel-
oping chlorophyll, and the tissue remaining succulent and form-

THE ENDOSPERM 179

ing intercellular spaces. A similar extensive growth and
escape of the endosperm is reported to occur during the germi-
nation of the seeds of Ricinus. In the germination of the seeds
of certain Piperaceae (Peperomia and Heckeria) Johnson ** 5%
has described the endosperm as bursting out of the seed-coat,
and continuing to jacket the embryo, which at germination is a
globular undifferentiated mass of cells, until the root, hypocotyl,
and cotyledons are organized. In the same papers Johnson ealls
attention to the fact that the endosperm of these Piperaceae
is not a storage region, but digests, absorbs, and passes on food
material to the embryo from the much more abundant. peri-
sperm, which is the real storage tissue. This restriction of the
function of the endosperm Johnson ** had already pointed out
in Saururus, and suggests the probability that this same relation
between endosperm and perisperm obtains in all seeds with
abundant perisperm as in Polygonaceae, Chenopodiaceae, Phy-
tolaccaceae, Caryophyllaceae, ete. The following quotation °°
will serve to make plain the author’s point of view:

‘Observations thus far made Jead me to believe that in the peri-
sperm-containing seeds mentioned the embryo sporophyte of the second
generation is never nourished by the parent sporophyte directly, but
always through the intermediate gametophyte. In general, then, we
find that the food substance supplied to the embryo by the nucellus
may pass through the endosperm and be stored in the embryo during
the ripening of the seed, as in Cucurbita and Phaseolus ; or, secondly,
the food may be stopped in transit between the nucellus and the embryo
and stored in the endosperm, there to be held during the resting period
of the seed and delivered over to the embryo only at the time of sprout-
ing, as in Ricinus, Zea, and apparently all Gymnosperms ; or, finally,
the food supply for the developing embryo may be stored in the nucel-
lus itself until the time of germination, when it is passed on to the
embryo through the endosperm, as in Saururus, Peperomia, Phyto-
lacca, Canna, and others.”

The phenomenon of xenia has a direct bearing upon any
discussion of the endosperm. The name was applied by Focke,®
in 1881, to the direct effect of pollen on seeds and fruits out-
side of the embryo, as shown in hybrids. The case of peas has
long been cited, but Giltay 1* has shown that the effects referred
to occur in the cotyledons, and therefore can not be considered
as xenia. So far as definitely known, the effect of foreign
pollen outside of the embryo is observed only in the endosperm,

186 MORPHOLOGY OF ANGIOSPERMS

as first pointed out by Kérnicke,? and this has been most clearly
established in the crossing of races of corn. It also appears
that this influence of foreign pollen extends only to the color
of the endosperm and the chemical composition of the reserve
materials, the size and form of the kernels remaining un-
changed, as stated by Correns.?° For example, if white or yel-
low corn be crossed with pollen from a red corn, many of the
resulting kernels will be red or variously mottled; or if sweet
corn, with its wrinkled and sugary endosperm, be crossed with
pollen from dent or flint corn, the result is smooth kernels with
starchy endosperm.

The possibility of such a direct effect of pollen was for a
long time questioned, and the phenomenon remained inexphi-
cable. With the discovery of ‘double fertilization ” or triple
fusion by Nawaschin 7? in 1898, the explanation of xenia oc-
curred simultaneously and independently to Correns,** De
Vries,?7 and Webber,*® the paper of the last investigator being
a very complete résumé and discussion of the subject based upon
his own extensive experimental work. To claim that the phe-
nomenon of xenia, as observed in corn, is due to the fusion of
one of the male nuclei with the primary endosperm nucleus was
an assumption, although an irresistible one, until such fusion
was demonstrated by Guignard #1 in 1901. It has been proved
repeatedly that when xenia occurs the embryo is a hybrid, so
that we have in xenia not only a hybrid endosperm, but a gross
demonstration of the occurrence and effect of the triple fusion,
and also an indication of the sort of characters that can be
brought into a structure by a male nucleus.

In many cases of xenia following the crossing of races of
different colors, the kernels are not of uniform color, but are
parti-colored or variously mottled. The ingenious explanation
suggested by Webber is that the male nucleus has failed to unite
with the fusion-nucleus and may be able to divide independ-
ently. If so, there would result two cel-races of different
characters that might be variously arranged with reference to
one another in the endosperm. It is entirely conceivable that
under favorable conditions of nutrition and physical environ-
nent an independent male nucleus may begin divisions, espe-
clally as this has been observed in the case of certain animals:
but it seems more probable that the independent appearance of

THE ENDOSPERM 181

these racial characters is due to the incompleteness of the triple
fusion, since it is well known that division of the primary endo-
sperm nucleus often begins before the constituent nuclei have
lost their identity. In fact, Webber calls attention to the begin-
ning of division before complete fusion in the case of the eggs
of certain animals, and the same is true of the sexual fusion-
nucleus of some Gymnosperms. An alternative hypothesis sug-
gested by Webber is that the male nucleus may fuse with one of
the polar nuclei, the other remaining independent and dividing.
These hypotheses are valuable in suggesting investigation as to
whether the male nucleus ever divides independently in the em-
bryo-sac, or whether it may unite with one polar nucleus, the
other dividing independently.

It remains to consider the morphological character of the
endosperm of Angiosperms. In view of the details as to its
origin and behavior given above, it is evident that it is a struc-
ture peculiarly difficult to interpret. The view has long been
held, dating from Hofmeister, that the endosperm is belated
vegetative tissue of the female gametophyte, stimulated in a
general way to develop by the act of fertilization, and in every
way the morphological equivalent of the structure bearing the

same name among Gymnosperms. Strasburger ** has suggested
that this postponement of the formation of endosperm is of
advantage in avoiding the waste that would follow its formation
and separation from the parent plant with every unfertilized
ovule. Of course the serious difficulty in this view of the nature
of the endosperm was that it offered no historical explanation
of the fusion of the polar nuclei. It could only claim that
fusions of vegetative nuclei, evidently resulting in growth-
stimulus, are by no means unknown, and in fact occur in the
endosperm itself. This view does not appear to have been
seriously disturbed by the claim of Le Monnier® in 1887, that
the fusion of the polar nuclei is a sexual process, and that there-
fore the endosperm is a second embryo modified to serve as
food tissue.

With the discovery of the fact that, at least in many cases,
a male nucleus enters into the organization of the primary endo-
sperm nucleus, the old view has been seriously menaced. The
commonly used phrases “ double fertilization” and ‘“ double
fecundation ” indicate general consent to the view that this

182 MORPHOLOGY OF ANGIOSPERMS

act of the male nucleus is a case of true fertilization, the infer-
ence being that the endosperm is a second embryo or sporophyte,
as Le Monnier had suggested.

Strasburger *7 in discussing the whole subject concludes that
the triple fusion is not real fertilization. Of course in such a
discussion much depends upon the definition of fertilization.
Strasburger distinguishes between “ generative fertilization ”
and “vegetative fertilization,” the former being a definite
union of parental qualities and resulting in an embryo, the
latter a fusion resulting merely in a growth-stimulus. He
thinks that the endosperm is historically a gametophyte, and
that the fusion which initiates it has no origin in an act of
fertilization.

Later, Miss Sargant ** published an admirable résumé of
the subject, together with a clear statement of the problems
involved and certain suggestions by way of interpretation. She
very justly states that if the endosperm “ arose from a belated
formation of prothallus, we must trace the origin of the triple
nuclear fusion which precedes its development”; and if it is
a modified embryo “ we have to account for the interference of
the lower polar nucleus with the act of fertilization, and for
the subsequent development of a body unlike a normal embryo.”
Her suggested interpretation of the phenomenon is that the

fusion of the male nucleus with the micropylar polar nucleus, an
undoubted female nucleus, both containing the reduced number
of chromosomes, is a typical sexual union; but that the antip-
odal polar nucleus, with its vegetative character, and indefi-
nite and usually increased number of chromosomes, is a disturb-
ing factor, and the result is not a normal embryo but a small
and short-lived mass of tissue. She aptly cites the experiments
of Boveri ** with sea-urchins, in foreing more than one sperm-
nucleus to unite with a single egg-nucleus and producing mon-
strous larval structures. ‘ The presence of the third nucleus,
therefore, with its redundant chromosomes, serves to secure the
degeneracy of the resulting tissue.

”

This means, of course, that
the endosperm is a degenerate embryo, and that the triple
fusion is a true sexual union whose normal result has been
interfered with by the presence of a non-sexual nucleus in the
combination,

It is impossible to solve such a problem by a discussion of

THE ENDOSPERM 183

the data we possess. The phylogeny of the endosperm must be
traced, and the place of the polar fusion and of the triple fusion
in its history determined before opinions cease to differ as to
its morphological character. In view of such facts as we have,
however, we are inclined to hold with Strasburger that the
endosperm of Angiosperms is a gametophytic structure, and
that the polar fusion and the triple fusion are interpolations
in its history that do not change its essential character. The
fact that endosperm sometimes forms before fertilization indi-
cates that the triple fusion is not an essential prerequisite; the
fact that endosperm forms without the polar fusion points at
least to the conclusion that it was once developed without it;
the indifference of the male nucleus as to which polar nucleus
it fuses with (Lilium, Asclepias) does not show the selective
attraction connected with sex-fusion; and the further fact that
when an undoubted fertilization occurs, whether of egg, of syn-
ergid, or of upper polar nucleus, an embryo is the result, indi-
cates that the presence of the male nucleus in triple fusion is of
subsidiary rather than of dominating importance. That the
fusing male nucleus does introduce parental characters that
manifest themselves in the endosperm is proved by the phenom-
enon of xenia, but this does not seem necessarily to prove the
sporophytic character of the endosperm. In fact, the develop-
ment and structure of the endosperm of Angiosperms is so much
like that of Gymnosperms that it seems easier to regard the
various fusions as merely resulting in a stimulus to growth than
to imagine a degenerate embryo assuming this particular de-
velopment and structure. Of course one might go to the ex-
treme, and regard the endosperm as neither gametophyte nor
sporophyte, but as a composite tissue involving both, but this
hardly seems to be necessary.

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nique 15: 37-50. 1901.
La double fécondation dans le Naias major. Jour. Bota-
nique 15: 205-213. figs. 14. 1901.
Double fécondation chez les Renonculacées. Jour. Bota-
nique 15: 394-408. figs. 16. 1901.

. HotFerty, G. M. Ovule and Embryo of Potamogeton natans.

Bot. Gazette 81: 339-346. pls. 2-3. 1901.

186 MORPHOLOGY OF ANGIOSPERMS

45.

46.

50.

51.

53.

54.

58.

60.

Lyon, H. L. Observations on the Embryogeny of Nelumbo.
Minn. Bot. Studies 2: 643-655. pls. 48-50. 1901.

SmitH, AMELIA C. The Structure and Parasitism of Aphyllon
uniflorum Gray. Contrib. Bot. Lab. Univ. Penn. 2: 111-121.
pls. 13-15, 1901.

. ScHNEGG, H. Beitrige zur Kenntniss der Gattung Gunnera.

Flora 90: 161-208. figs. 28. 1902.

. GUIGNARD, L. La double fécondation chez les Solanées. Jour.

Botanique 16: 145-167. figs. 45. 1902.

. StraspurGerR, E. Ein Beitrag zur Kenntniss von Ceratophyllum

submersum und phylogenetische Erérterungen. Jahrb. Wiss.
Bot. 87: 477-526. pls. 9-11. 1902.

Hau, J.G. An Embryological Study of Limnocharis emargi-
nata. Bot. Gazette 33:°214-219. pl. 9. 1902.

OveERTON, J. B. Parthenogenesis in Thalictrum purpurascens.
Bot. Gazette 33: 363-375. pls. 12-13. 1902.

2. Cook, M. T. Development of the Embryo-sac and Embryo of

Castalia odorata and Nymphaeaadvena. Bull. Torr. Bot. Club
29: 211-220. pls. 12-13. 1902.

Jounson, D.S. The Embryology and Germination of the Genus
Peperomia. Abstract. Science 15: 408-409. 1902.

Ikepa, T. Studies in the Physiological Functions of Antipodals
and related Phenomena of Fertilization in Liliaceae. 1. Tricyr-
tis hirta, Bull. Coll. Agric. Imp. Univ. Tokyo 5: 41-72. pis.
3-6, 1902.

. JoHNson, D. 8. On the Development of Certain Piperaceae. Bot.

Gazette 84: 321-340. pls. 9-10. 1902.

3. Frye, T. C. A Morphological Study of Certain Asclepiadaceae.

Bot. Gazette 84: 389-413. pls. 15-15, 1902.

. SarpaTa, kK. Experimentelle Studien jiber die Entwickelung des

Endosperms bei Monotropa. (Vorliiufige Mitteilung.) Biol.
Centralbl. 22: 705-714. 1902.

MuRBECK, 8. Ueber die Embryologie yon Ruppia rostellata
Koch. K6nigl. Svensk. Vetensk. Akad. Tandl, 36: 1-21. pls.
I-85, 1902.

. Frye, T.C. The Embryo-sac of Casuarina stricta. To be pub-

lished in Bot. Gazette 35: 1903.
Wvyuir, R. B. A Morphological Study of Hlodea canadensis. To
be published in Bot. Gazette 36: 1903.

CHAPTER

IX

THE EMBRYO

Ir is perhaps impossible at present to formulate any defi-
nite laws for the development of the embryo of Angiosperms.

The details recorded are very nu-
merous and confusing, the great-
est amount of variation occurring
in allied forms and even in the
same species. Undue attention
probably has been given to the
succession of cell divisions in the
earliest stages of the embryo, for it
is at this very period that the em-
bryo seems to be peculiarly respon-
sive to the conditions that surround
it. What the conditions are that
determine that a cell-wall in a
given stage of the embryo shall
run now in one plane, now in an-
other, or even shall fail to develop,
are unknown; but the study of a
large series of embryos makes it
evident that if there is a normal
sequence of cell divisions it is
being constantly interfered with.
It is probable that when these
minor variations are neglected, cer-
tain laws of general development
will appear that are concerned with

Fie. 81.—Capsella Bursa - pastoris.
Photomicrograph of seed showing
embryo, endosperm, and develop-
ing testa; x 125.

the organization of the great body regions rather than with the
succession of cell divisions (Fig. 81).

187

MORPHOLOGY OF ANGIOSPERMS

a
(oa)
Dm

In general, the first division of the fertilized egg is trans-
verse, and this is followed by one or more divisions in parallel
planes, resulting in a row of cells. This undifferentiated group
of cells is conveniently referred to as the proembryo. In gen-
eral, the proembryo becomes differentiated into suspensor and
embryo, which eventually become very distinct, although their
origin is variable. This means that in general all the product
of the fertilized egg does not enter into the structure of the
embryo, a fact also true of most Gymnosperms. In general,
the development of the embryo is initiated by the longitudinal
division of the end-cell of the proembryo, and this is followed
by divisions that result in the quadrant and then the octant
stage. It is in the octant stage that periclinal walls may cut off
the dermatogen, but this may be deferred to a later stage, and
is often irregular. The cells of the dermatogen divide only by
anticlinal walls, but the inner cells continue divisions in the
three dimensions, and soon the periblem and plerome become
distinguishable. In general, the end-cell of the proembryo does
not produce all of the embryo, but the next cell divides trans-
versely, and the daughter-cell adjacent to the embryo (h ypo-
physis) fills out the periblem and dermatogen of the root- tip.
The organization of the growing points of stem and cotyledon,
in relation to the body of the embryo, are so radically different
in Monocotyledons and Dicotyledons that no general statement
concerning it is possible.

The fact remains that every general statement given above
is contradicted by well-known and by no means infrequent ex-
ceptions, and even the distinction betw een Monocotyledons and
Dicotyledons is not always clear in the embr vo. The subject
will be treated in some detail under the titles Monocotyledons,
Dicotyledons, Parthenogenesis, and Polyembryony.

MONOCOTYLEDONS

The embryo of Alisma Plantago, as described by Hanstein 7
and Famintzin,!? has long been taken as a type of thie monocot-
yledonous embryo. Among recent accounts Schaftner’s #8 de-
scription of the embryo Sagitlaria variabilis, felines his
earher study of Alisma®” is the most complete, and while it
confirins the prine ipal features of the earlier accounts, the ereat
improvement in technique since the time of Hanstein made it

Fic. 82.—Sagittaria variabilis. Development of embryo. A, proembryo of three cells;
a, basal cell (in all figures) ; 6, middle cell (dividing); ¢, terminal cell from which
the cotyledon is derived; sy, synergid; B, same stage, but terminal cell dividing ;
C, middle cell (6) has divided, s being the cell from whose derivatives the stem-tip
arises, and terminal cell (¢) dividing; D, both cells derived from 6 are dividing;
£, terminal cell has given rise to four cells (c), and the region derived from the
middle cell (6) has developed further; F, showing further development of the
middle cell region (4), while the terminal cell region has made no further progress ;
G, dermatogen differentiated in the terminal cell region (c), and the middle region
(}) further developed; Z, differentiation of dermatogen beyond the terminal region
(c), the middle region (6) showing the differentiation between hypocotyl (/) and
region producing stem-tip; J, more advanced stage, showing same regions as in H,
but the dermatogen of the root-tip not yet formed, and the plerome and periblem
undifferentiated. A-F, x 400; G, x 260; H, x 400; Z, x 260.—After ScHAFFNER.43

189

190 MORPHOLOGY OF ANGIOSPERMS

possible to correct some inaccuracies, and at the same time to
show that the early divisions of the fertilized egg do not follow
such a definite sequence as had been supposed. The following
description is based upon his account. The fertilized egg di-
vides by a transverse wall, and the resulting basal cell becomes
large and vesicular, but does not divide. The apical cell divides
by a transverse wall and a proembryo of three cells is the result
(Fig. 82). The terminal cell (Fig. 82, ¢) gives rise to the ter-
minal cotyledon, and its first division, which may take place im-
mediately or may be somewhat delayed, is always longitudinal.
From the middle cell there are developed the lateral stem-tip,
the root-tip, the hypocotyl, and all of the suspensor except the
vesicular basal cell. The middle cell divides transversely, and
of the two resulting cells the one next the terminal cell gives rise
to the stem-tip (Fig. 82, C, s). In general, the differentiation
is basipetal, proceeding from the cotyledon toward the suspen-
sor. The terminal or cotyledon cell having divided by a longi-
tudinal wall, the next division is transverse, resulting in the
quadrant stage, followed by the octant stage. At this stage
the dermatogen begins to be differentiated, appearing first in
the cotyledon and proceeding toward the root end of the em-
bryo. While the cell from which the stem-tip arises can be
identified in the four-celled proembryo, it is only in much later
stages (as Fig. 82, £) that it is readily recognized. In the
four-celled proembryo (Fig. 82, C’) the cell next the vesicular
cell divides transversely ; and of the two resulting cells the one
nearest the vesicular cell by one or more transverse divisions
gives rise to a filamentous suspensor of two to six cells: from
the other cell are developed the root and the hypocotyl. The
dermatogen is usually developed, even around the root-tip, be-
fore any differentiation of periblem and plerome ean be dis-
tinguished (Fig. 83),

This Alisma type has proved to be characteristic, not of
Monocotyledons in general, but of the more primitive hydro-
phytic forms, Its main features are an undividing and usually
much enlarged and swollen basal cell cut off by the first division
of the fertilized ege, and a proembryo of three cells whose mid-
dle cell divides basipetally to form the region of the embryo
behind the cotyledon, and also forms more or less of a suspensor
in addition to the large basal cell. As further illustrations of

Fie. 83.—Sagittaria variabilis. Development of embryo. 4,somewhat advanced stage
showing the depression in which the stem-tip develops; x 216; B, about the same
stage, showing the entire embryo; x 66; @, later stage, with dermatogen, periblem,
and plerome differentiated; x 216; D, the lateral stem-tip; x 140; £, longitudinal
section of a ripe seed; x 26.—After Scuarrner.‘9

191

192 MORPHOLOGY OF ANGIOSPERMS

it we would cite Sparganium (Campbell®*), Potamogeton
(Wiegand, Holferty™), Zannichellia and Naias (Camp-
bell 1), Lriglochin (Hill ®°), and Limnocharis (Hall **). The
last-mentioned form well illustrates that the general type may
be maintained, and at the same time there may he no regularity
in the sequence of divisions after the first two. In fact, the
apical cell of the proembryo of Limnocharis may divide by a
transverse, oblique, or longitudinal wall, and in the two latter
cases the cotyledon and stem-tip are both terminal, as is the
case also in Zannichellia.

Among the Gramineae the same general type of proembryo
is formed, but if Avena fatua (Cannon ®*) be taken as repre-
sentative of the general situation, the origin of the organs of
the embryo in relation to the cells of the proembryo is quite
different. In this species the cotyledon and stem-tip are both
derived from the apical cell, the entire root-tip (including root-
cap) from the adjacent cell, and the coleorhiza from the third
cell, the suspensor consisting of only the primary basal cell.

Among the Araceae a very different type of embryo is indi-
cated, but so few forms have been investigated that no conclu-
sion as to its prevalence in the family is safe. In 1874 Hegel-
maier ® described the absence of
a suspensor in Pistia, the tertil-
ized egg producing a spherical
proembryo, all of which enters
into the structure of the embryo.
Campbell ** found the same type
of embryo in Dieffenbachia, Ag-
laonema, and Lysichiton (Fig.
84+), and states that in the seg-
mentation of the egg there may
be two transverse divisions be-

fore any vertical division, or a
Fie, 84.— Lysichiton kamtschatcense. yeoular quadrant may be formed
Longitudinal section of embryo sur-
rounded by endosperm, illustrating A : seeps
the Pistia type.—After CampReiy. 55 Even if this Pistia type should

prove to be characteristic of the
Araceae, it is not restricted to them, for Tumphrey *8 has
shown that the embryos of the Scitamineae have no suspensors ;
and the same is true at least of certain orchids, as shown bv

as in the ordinary fern embryo.

THE EMBRYO 193

Treub** for Listera ovata and Epipactis palustris, and by
Leavitt ‘* for certain species of Goodyera and Spiranthes. It
should be noted, however, that in Lemna (Caldwell **), the

reduced aquatic ally
ot the Araceae, a mul-
ticellular suspensor is
formed, the embryo
resembling the Lili-
um type described be-
low.

Among the Lilia-
ceae a third type of
embryo-formation
seemstoprevail. After
the first segmentation
of the fertilized ege,
which is transverse,
the subsequent divi-
sions are very irregu-
lar, being transverse,
oblique, or longitudi-
nal in either cell, re-
sulting in a massive
proembryo. The dit-
ferentiation into em-
bryo and suspensor is
late and irregular, the
suspensor being mass-
ive, and inclined to
continue active divi-
sion until the end of
the embryo-sac is oc-
cupied by a spreading

suspensor tissue (Fig.

Fie. 85.—Lilium philadelphicum. A, proembryo of
two cells; x 300; B, middle cell of filament of
three cells has divided longitudinally; x 175; @,
young embryo showing massive suspensor; x 300;
D, older embryo, showing different form of sus-
pensor ; x 300.—After CouLTEr.“#

85). This is characteristic of Lilium

(Coulter #4), Erythronium (Schaffner ™), Tulipa (Ernst %),
and probably all the allied forms, and the meristematic activity
of the suspensor is apt to result in polyembryony (see below).
Just how far this Liliwm type of embryo is represented among
Liliales must be determined by future investigation, but it is
distinct enough to deserve separate mention.

194 MORPHOLOGY OF ANGIOSPERMS

Among the Orchidaceae there is the greatest amount of
variation in the formation of the embryo. In general they are

characterized by very poorly developed em-

bryos, the body regions not being differen-
tiated, and by an extraordinary and varied
development of the suspensor as an hausto-

rium. As already mentioned, however, some

of them (species of Listera, Epipactis, CGlood-

Fia. 86.—Listera ovata.

yera, Spiranthes) have no suspensor (Fig. gmbryo at time of

Fia. 87.— Gymnadenia conopsea.
Section of embryo with suspen-
sor protruding from micropyle.
—After Marsnate Wanrp.2o

86). Treub 1% in shedding seed. After
1879: degetibed 9 2S. Haute
ati " and Prantl’s Vat.
number of forms in Pflanzenfamilien.
which the filamen-
tous suspensor grows out of the micro-
pyle, often branches, and embeds it-
self in adjacent nutritive tissue, such
as the placenta. He found that in
Phalaenopsis grandiflora branches of
the suspensor not only turn toward
the micropyle, but also toward the
embryo and finally envelop it. Later
the same investigator ** deseribed the
suspensor of Peristylis grandis as
dividing transversely, growing out
through the micropyle, and embed-
ding itself by psendopodium-like proe-
esses in the placenta. The embryo
of Gymnadenia conopsea, as described
by Marshall-Ward,*° is probably rep-
resentative. The first division of the
fertilized ege is transverse, the basal
cell forming a chain-like suspensor of
eight to ten more or less elongated
cells that pushes through the micro-
pyle into the ovary eavity, and the
apical cell producing a perfect octant
stage, the dermatogen being cut off
in the sixteen-celled stage (Fig. 87).
Leavitt * has also deseribed the sus-
pensors of Aplectrum hiemale; of

THE EMBRYO 195

Corallorhiza multiflora, in which it consists of two very long
cells and embeds its tip into the placenta; of Habenaria tri-
dentata, and of H. blephariglottis, in which each of the six or
seven cells of the suspensor usually sends out a branch, some of
them short and reaching the integument, others elongated and
passing parallel with the suspensor into the tissue at the base
of the funiculus.

These four types of monocotyledonous embryos, which for
convenience may be spoken of as Alisma, Pistia, Lilium, and
Orchid types, are, of course, related to one another in ways that
suggest that they are all derivatives of one general monocotyled-
onous form. It is natural to assume that this primitive form
is more nearly represented by the Alisma type than by any of

A

Fic. 88.—Zannichellia palustris. Development of embryo. A, young embryo; x 320;
BS, later stage, showing beginning of differentiation into stem-tip (s) and cotyledon (c),
both coming from the cells derived from terminal cell of proembryo; x 160; C, stem-
tip (s) and cotyledon (c) clearly differentiated; x 60.—After CampBELu.*t

the others, not merely because it characterizes the primitive
hydrophytic forms, but also because it is the simplest type,
and the others may well be modifications of it. In the Pistia
type the suspensor is suppressed ; in the Lilium type it becomes
massive and meristematic; in the Orchid type it 1s developed
as a special haustorium that passes out of the ovule on account
of the lack of endosperm, and perhaps for the same reason the
embryo does not reach the stage of differentiating organs. ‘

There have been observed certain departures from the mon-
ocotyledonous type of embryo that deserve special mention.

196 MORPHOLOGY OF ANGIOSPERMS

In 1878 Solms-Laubach !* stated that in Dioscoreaceae and
certain Commelinaceae the cotyledon is lateral in origin rather
than terminal. The stem-tip is terminal in origin, but is later
forced to one side by the strong growth of the cotyledon from
beneath. Such a departure is, of course, fundamental, but be-
fore any generalization is ventured it should be subjected to the
most critical investigation, Campbell *! finds that in Zanni-
chellia the terminal cell of the proembryo gives rise to both coty-
ledon and stem-tip, the separation between the two organs being
determined by the first vertical division of the terminal cell
(Fig. 88). The same writer *7 has found another suggestive
variation in Lilaea subulata, one of the Juncaginaceae. The
embryonic root-tip, instead of being directed toward the sus-
pensor, is directed to one side, almost in continuation of the
axis of the stem-tip. This lateral origin of the root is regarded
by Campbell as a primitive feature, and suggestive to him of
Tsoetes. In other particulars the embryo is of the Alisma type.
In this connection the recent results of Murbeck °° with Ruppia
are suggestive. He confirms the account of Wille that a pri-
mary root is formed at the base of the embryo, but soon dis-
organizes, and that a lateral root, formed very early, is the first
functional one. This is very different from the account of
Ascherson in Engler and Prantl’s ‘ Die Natiirlichen Pflanzen-
familien,” which is followed in Goebel’s “ Organography,” ac-
cording to which this lateral root is the primary root, its wn-
usual position being due to displacement.

DICOTYLEDONS

The best-known dicotyledonous embryo is that of C apsella,
as described by Hanstein? and Famintzin, 7 and it has nee
used as a basis of comparison ever since. To illustrate the
earlier stages in the development of the embryo, therefore, we
have made a rather complete series of camera drawings from
sections of the embryo of Capsella (Figs. 89, 90: see also Fig.
81). The proembryo is a filament of cells of varying length.
The apical cell divides first longitudinally, the next two divi-
sions being longitudinal and transverse in either order and
resulting in the octant stage. Whether the transverse division
precedes or follows the second longitudinal division, it se pa-
rates the cotyledonary and hypocotyledonary regions of the em-

Fie. 89.—Capsella Bursa-pastoris. A, first division of terminal (embryo) cell; B, quad-
rant stage; (, octant stage; J, differentiation of dermatogen; £, differentiation
of periblem and plerome (latter shaded); 7, completion of periblem of root; G,
beginning of differentiation of dermatogen of root-tip (indicated by mitotic figure) ;
H, later stage, showing plerome, periblem, dermatogen, and one layer of root-cap
(plerome and dermatogen shaded); J, two layers in root-cap (the plerome and
portion of dermatogen derived from hypophysis shaded); J, young embryo sur-
rounded by endosperm; walls of ovary also shown; x 400.

197

198 MORPHOLOGY OF ANGIOSPERMS

bryo. In the octant stage the dermatogen begins to be differ-
entiated, the periclinal divisions appearing first in the terminal
octants and proceeding toward the root end of the embryo. The
differentiation, however, is almost simultaneous, so that the
dermatogen is soon completed except that of the root-tip, which
is derived from the adjacent cell of the suspensor, and appears
comparatively late. The periblem and plerome are differen-
tiated early from the tissue within the dermatogen. The stem-
tip and cotyledons are derived from the four apical octants, and
the bulk of the hypocotyl from the four basal octants. The
root-tip, however, is completed by the adjacent cell of the sus-

Fig. 90.— Capsella Bursa-pastoris. Series showing contribution of upper cell of suspen-
sor to embryo (plerome and dermatogen shaded): s, upper cell of suspensor; /,
hypophysis; d, dermatogen; ¢@’, portion of dermatogen derived from hypophysis ;
pl, plerome; p, periblem ; p’, portion of periblem derived from hypophysis ; x 400.

pensor (Fig. 90, s). This cell divides transversely, the basal
daughter-cell taking no part in the formation of the embryo,
but the other daughter-cell (hypophysis of Ianstein) filling
out the periblem and dermatogen of the root-tip. The hypophy-
sis divides transversely, the daughter-cell next the embryo com-
pleting the periblem of the root. The other daughter-cell by
two longitudinal divisions gives rise to a plate of four cells,
each of which divides transversely, the plate of four cells toward
the embryo completing the dermatogen of the root-tip, and the
other plate constituting the first layer of the root-cap.

THE EMBRYO

199

This type of embryo, called for convenience the Capsella
type, is well represented throughout the Dicotyledons, and, so

far as we have the means to judge,
seems to be the prevalent type, subject,
of course, to variation in detail. For
example, it occurs in Salix (Chamber-
lain #7), in which it is questionable
whether the hypophysis contributes to
the periblem; in Ranunculus (Coul-
ter**) and Thalictrum (Overton **),
in the latter case the suspensor some-
times becoming a massive and twisted
organ; in Adyssum (Riddle *1), which
almost exactly repeats the embryogeny
of Capsella; in Stum, mm which there
is a very long suspensor; in Sarcodes
(Oliver °°); in Avicennia (Treub **) ;
in T'rapella (Oliver *”), in which there
is a remarkably long suspensor with an
enormously elongated basal cell; and in
Senecio (Mottier **), Stlphium (Mer-
rell®), and Taraxacum (Schwere *°).
Among the Rosaceae Péchoutre ** has
recorded a wide variation in the struc-
ture of the suspensor, different genera
showing every gradation between a sim-
ple filamentous suspensor (Pragaria,
Geum) and one that is short and mass-
ive ( Crataegus, Amygdalus). These
examples represent all regions of Dicot-
vledons; and while there are differ-
ences as to the division of the basal
suspensor-cell, the length of the sus-
pensor, and the succession of walls in
the apical cell (embryo-cell) of the pro-
embryo, the general type remains the
same, and resembles most nearly the
Alisma type among Monocotyledons.
Tn addition to this prevailing type,
there are modifications of it that sug-
14

B

Fie. 91.— Loranthus sphaero-
carpus. A, young embryo;
x 190; B, later stage, show-
ing extreme lengthening of
the two bulbous suspensor-
cells; ¢, embryo; s, suspen-
sor; x 120.—After TREUB.??

200 MORPHOLOGY OF ANGIOSPERMS

gest as wide a range of variation as among Monocotyledons,
though not so clearly related to great groups.

In Geranium, as has long been known, while the Capsella
type is maintained in general, there is no hypophysis, the root-
tip being covered by the tissue of a massive suspensor.

In Peperomia pelluctda Campbell °® and Johnson °° have
both observed that the first segmentation of the fertilized egg
is vertical, followed by a transverse division, and that there is
no indication of a suspensor. ?

In Loranthus sphaerocarpus Treub ** has described the first
division of the fertilized egg as vertical, as in Peperomia, but
followed by transverse divisions, so that the proembryo resem-
bles two filaments lying side by side (Fig. 91). The two basal
cells elongate enormously, forming a suspensor as In Gymno-
sperms, whose length is increased by the moderate elongation
of the second pair of cells, and which becomes more or less tor-
tuous, the cells twisting about one another. In L. pentandrus
(Treub **) the elongating suspensor early forces the embryo
against the resistant base of the sac, where it becomes much
flattened out, and for a time bears little resemblance to an em-

Fia. 92.— Loranthus pentandrus. A, young embryo advancing into endosperm ; thiek-
walled tissue at base of sac deeply shaded; e, embryo; s, suspensor; x Ss; B later
stage, the embryo has reached the resistant base of the sac and has beeome flattened
out; « 144—After Treup.26

bryo (Fig. 92). In Myoporum, as deseribed by Billines.7° the
suspensor is also extremely long and filamentous, forcing the
young embryo down into the principal mass of endosperm,

THE EMBRYO 201

which is at a considerable distance from the micropylar end
of the embryo-sae (Fig. 93).

In Nelumbo Lyon states that there is no suspensor, but
that the divisions of the ege result in a large spherical body
that is still undifferentiated when
consisting of several hundred cells,
recalling the Pistia type among
Monocotyledons. In Ceratophyl-
lum demersum Strasburger **+ has
found the same undifferentiated

Fie. 93.— Myoporum serratum. Young Fie. 94.—Barringtonia Vrieset. A, young
embryo with very long suspensor proembryo; &, later stage, showing
embedded in endosperm. — After differentiation into embryo (e) and
BI.iiées.7° suspensor (s); x 104.—After Treus.7

spherical embryo of hundreds of cells and with no suspen-
sor; while in Nymphaea Conard *! finds the same type, but
associated with it is a suspensor consisting of a row of
three to five cells. In Heckeria (Piperaceae) Johnson ** has
described the early stage of the embryo as a globular mass
composed of several hundred cells undifferentiated except for
a rudimentary suspensor ; and in Cynomorium ( Balanophora-
ceae) Juel®* describes the embryo as a small spherical mass
of cells with no suspensor and no differentiation into body
regions.

In Barringtonia Vriesei, one of the Myrtaceae, Treub 77
has described a broad mass of tissue almost filling the micropy-
lar end of the embryo-sac. At first the mass is homogeneous,

bo

20 MORPHOLOGY OF ANGIOSPERMS
and it is only late that the embryo becomes differentiated from
the massive suspensor (lig. 9+).

In the Rubiaceae Lloyd **: ** has described a remarkable de-
velopment of the suspensor, which in many members of the group
acts as a haustori-
um (Fig. 95). In
Vaillantia hispida
the large suspensor
cells near the em-
bryo are clustered
like ‘fa buneh of
erapes,” while far-
ther down a single
elongated cell forms
a point of attach-
ment. In Asperula
the scanty cyto-
plasm and the nu-
cleus are found at
the distal ends of
the haustorial cells

Fie. 95.—4, Vaillantia hispida. Young embryo showing of the suspensor,
haustorial suspensor; x 5753; after Luoyn.o? By Aspe- recalling a eondi-
rula azurea, Young embryo with haustoria from sus-

tion which has been
pensor highly developed ; after LLoyp.%°

described for root
hairs. It is worthy of note that among the Spermacoceae and
in Foustonia there is a complete absence of these striking
adaptive characters of the suspensor.

It is among the Leguminosae, however, that the greatest
amount of variation in embryogeny exists and the most unusual
forms appear, as shown by Guignard *! (Figs. 96-98). It is
impossible to give in a brief account any adequate idea of the
amount of variation displayed by the nearly forty species Guig-
nard has deseribed, involving in the main the character of the
prociubryo and the final condition of the suspensor. In 1880
Strasburger 1? had called attention to the fact that the cells of
the very long suspensor of Lupinus separate early, leaving the
embryo free and some distance from the mieropylar extremity
of the sac. This, however, is but one phase of the embrvogeny
of the Leguminosae. In every case the first segmentation of the

THE EMBRYO 208

egg is transverse, but this may be followed either by longi-
tudinal or transverse divisions, in the former case generally re-
sulting in a massive and often globular proembryo, in the latter
resulting in an extraordinarily long and conspicuous filamen-
tous proembryo. In almost every case the suspensor-cells are
more or less swollen and bladdery and surcharged with nutritive
material, forming a conspicuous nutritive tissue for the embryo.
The two types of proembryo may be illustrated as follows:

As illustrations of the massive proembryo, in which the sus-
pensor and embryo are gradually differentiated, but are never
very distinct externally except by a constriction between them,
may be cited species of Acacia and Mimosa; Cercis siliquas-
trum, in which the oblong proembryonic mass broadens at each
end to form the embryo and suspensor ; Caesalpinia mimosoides,
in which the embryo becomes distinct rather early as the region
of more actively dividing cells; Cytisus Laburnum, in which
the suspensor becomes a great mass of loose rounded cells re-
sembling a globular cluster of berries; Anthyllis tetraphylla,
in which the suspensor is like that of Cytisus, but the clustered

=e

Fic. 96.—Embryos of Leguminosae. A, Cercis siliquastrum, with suspensor and embryo
developing about equally; x 270; B-4, Spartium junceum : e, embryo; 8, suspen-
sor; x 800.—After GuIGNARD.?!

cells are much fewer in number; Spartium junceum and Trifo-
lium resupinatum, in which the massive proembryo seems to
constrict as in Cercis, but the suspensor as the cotyledon stage
approaches is smaller than the embryo; Tetragonolobus pur-
pureus, in which the larger part of the massive proembryo be-
comes the suspensor ; Hedysarum coronarium and Arachis hypo-

204 MORPHOLOGY OF ANGIOSPERMS

gaca; Onobrychis petraca, in which the proembryo is a globular
mass of cells; and Phaseolus multiflorus and Brythrina crista-
galli, in which the massive pro-
embryo is elongated and there
is no superficial separation be-
tween embryo and suspensor.
In ease two or more of the
first divisions are transverse,
forming a filamentous proem-
brvo, the end-cell forms the en-
tire embryo, the suspensor-cells
becoming relatively extremely
large and bladdery inflated.
Two general types may be noted.
In Orobus angustifolius, O. au-
reus, Pisum sativum, Lathyrus
heterophyllus, L. odoratus, Er-
ovum Ervilia, and Vicia narbon-
nensis, a proembryo consisting
of a row of three cells divides
longitudinally; the two basal
eells beeome mueh elongated,

Fie. 97.—Embryos of Leguminosae. 4, bladdery inflated, and multinu-

Orobus angustifolius, with suspenso. Cleate; the middle pair become
Be eae a eeeeape ace 336. bladdery inflated and multinn-
ci head ae en gen ae eleate; and at the end of such a
(e); x 160.—After Guianarp.2! suspensor the terminal par ot
cells organize a small round,

oval, or elongated embryo. In Cicer arietinum it is interesting
to note that the same huge suspensor and small embryo appear,
but the suspensor-cells instead of becoming multinueleate
divide, forming a many-celled massive suspensor. In the other
type, transverse divisions continue until the proembryo consists
of a long filament of cells, all of which, excepting the end-cell,
form a suspensor, as in Medicago falcata; Galega orientalis, im
which the long suspensor finally becomes massive by longitu-
dinal divisions; and OQnonis fruticosa, in which the suspensor-
eclls become very large and rounded, forming a chain that
finally breaks up. In Ononis alopecuroides, lhowever, the sus-

pensor is reduced to a single cell. The genus Lupinus is espe-

THE EMBRYO 205

cially characterized by its extensive, worm-like, and large-celled
suspensors, Whose cells often break apart. The suspensor may
consist of twenty pairs of elongated cells, forming a tortuous
filament extending the entire length of the embryo-sac, with a
very small embryo at the tip, as in L. swhcarnosus; or it may be
a filament of short, very broad cells, suggesting a leech in ap-
pearance, as in L. pilosus; or it may be a loose, large-celled
tissue lying along the cavity of the embryo-sac, actively dividing
and more or less surrounding the late-forming embryo with its
rounded cells, that finally break apart and become disorganized,
as in L. polyphyllus, L. mutabilis, L. truncatus, ete.

The degree of development of the embryo is extremely vari
able. In some cases a plumule with several leaves is formed, and

Fie. 98.—Embryos of Leguminosae. A, Lupinus subcarnosus, with long sinuous sus-
pensor and small four-celled embryo (¢); x 270. B, L. luteus, with many suspensor-
cells binucleate; x 160. ©, L. pilosus, with some basal suspensor-cells isolated ;

x 80,.—After GuIGNARD.?!

even lateral roots appear, as in Gramineae, Impatiens, Cucur-
bita, Trapa, ete.; while in many parasites and saprophytes the
embryo is represented only by an undifferentiated mass of cells.

200 MORPHOLOGY OF ANGIOSPERMS

Among the Monocotyledons such undifferentiated embryos ap-
pear among Orchidaceae and Burmanniaceae, in the former
family the primary root never appearing; but they are even
more numerous among Dicotyledons. Goebel ** states that the
embryo of Monotropa consists of five to nine cells, and that of
Pyrola secunda, quoting from Hofmeister, of eight to sixteen
cells. The entirely undifferentiated embryo of Aphyllon unt-
florum has been noted by Miss Smith‘; and the embryos of
Orobanchaceae (Koch !+), and of Balanophoraceae and Cytina-
ceae (Solms-Laubach *), consist of a very small mass of tissue.
In this connection it should be noted, however, that in Cuscuta
and Viscwm the embryos are large and well developed. In
some non-parasitie forms also poorly developed embryos occur,
as in Utricularia (KXamienski?!), in which the embryo develops
no root-tip but produces a large number of peculiar leaves.

The appearance of a single cotyledon in the embryos of
certain Dicotyledons has naturally attracted attention. As a
prefatory illustration, it may be observed that in Vrapa natans,
one cotyledon is much smaller than the other, and this suggests
the possibility of further abortion and even of suppression of
one of the cotyledons. In Ranunculus Picaria Irmisch? long
ago reported the occurrence of a single cotyledon sheathing
below, and Bizanthis hiemalis, Corydalis cava, and Carum
(Bunium) bilbocastanum have also been inelided in the list
of “ pseudo-monocotyledons.” In the ease of C. bulbocastanum
Hegelmaier !° discovered that the apparently single and ter-
minal cotyledon is accompanied by a second almost completely
aborted and lateral cotyledon. All of these forms have been
investigated recently by Schimid,®! who discovered that in Bri-
anthis hiemalis the two cotyledons are of unequal size: that in
Ranunculus Ficaria there is hardly a trace of a second cotvle-
don, and that this trace was probably mistaken by Irmisch 2
for a sheathing base; and that in Corydalis cava there is only a
slight protuberance to represent the second eotyledon, the fune-
tioning one in its growth eradually assuming a more terminal
position and thrusting the stem-tip to an apparently lateral posi-
tion, but in C. nobilis and C. lutea the normal development of
cotyledons is found. = In Cyclamen persicum, also, Schmid
found embryos m ripe seeds with no trace of a second cotyle-
don. From these cases it is evident that in certain dieotyled-

THE EMBRYO 207

onous forms there may be early abortion, which may even
approach suppression, of one of the cotyledons; and that in
consequence of this the single functional cotyledon may appear
terminal and the stem-tip lateral. To call such cases ‘ pseudo-
monocotyledons,” however, is not consistent with the real nature
of the monocotyledonous embryo. It is of interest to note, how-
ever, that Miss Sargant,** in her recent study of the ‘ mono-
cotyledonous Dicotyledons,” a special case being made of Ranun-
culus Ficaria, has concluded that the apparently single cotyle-
don is a fusion of two.

The peculiar development of the cotyledons of Nelumbo has
suggested to Lyon’ ™ that they represent a single two-lobed
cotyledon, and that this fact, along with certain anatomical
details, should place Nelumbo among the Monocotyledons. In
its early stage he represents the proembryo as being a many-
celled spherical body, that later becomes a flattened mass filling
the micropylar extremity of the sac. The stem-tip arises from
the free surface toward one side, and a cotyledonary ridge
arises behind it as a crescentic mound of tissue, whose wings
finally extending around form a sheath about the stem-tip.
By the development of two growing points on this cotyled-
onary sheath two lobes appear and develop rapidly, the two
becoming concave and surrounding the plumule as a tube. The
evidence in favor of a single cotyledon seems convincing until
this embryogeny is compared with that of Mymphaea, as has
been done by Conard.*! In'this genus the same spherical mul-
ticellular proembryo appears, two opposite and syminetrical
cotyledons with the stem-tip between them arising from the free
side, and the basal portion forming the hypocotyl. At maturity
the cotyledons become concave and inclose the plumule, just
asin Nelumbo. There can be no question that the two genera
are closely related; and since the embryogeny of Nymphaea is
typically dicotyledonous, it follows that that of Neliwmbo must
be only a modification of it, and that for some reason the stem-
tip does not occupy its usual central position, and the two
cotyledons arise for a time en masse, as in the case of petals
in sympetaly. Conard calls attention to such behavior on the
part of the cotyledons of Tropaeolum, which appear “ connate-
perfoliate ” about the hypocotyl]; and also to the fact that Hegel-
maier noted the complete fusion of the cotyledons along one

208 MORPHOLOGY OF ANGIOSPERMS

edge in Vuphar lutea. In his recent study of Ceralophyllum
Strasburger ** finds that the embryo in its earlier stages bears
a striking resemblance to that of Velwmbo, there being a large
spherical mass of cells with no suspensor (Fig. 80). The em-
bryo of Velumbo has the rudiment of a root, although it never
develops, the first functional roots coming from the stem above
the cotyledon (Fig. 50, 8). In Ceratophylliun the reduction
due to the water habit has gone further, not even the rudiment
of a root appearing in the embryo. The two cotyledons of
Ceratophyllum so strongly resemble the condition.in Nelumbo,
that Strasburger, after examining the embryo of the latter, was
forced to believe that here also, as in Ceratophyllum, there are
two cotyledons.

The occasional occurrence of a whorl of three cotyledons
has been reported for Quercus, Amygdalus, Phaseolus, ete., and
many other eases are given by Braun.®

Jn this connection, recent suggestions as to the phylogeny
of the cotyledon may be referred to. The current opinion re-
gards it as a modified foliage leaf, and this is borne out in the
majority of Dicotyledons by the assumption of the foliage fune-
tion. The terminal cotyledon of Monocotvledons, however,
seems to belong to a different category, and to hold no relation
to a foliage leaf or to a foliar member of any description. In
a recent paper IT. L. Lyon ** develops the idea that the cotvle-
don of Angiosperms is phylogenetically related to the sucking
organ known as the “foot? among Bryophytes and Pterido-
phytes. His own summary makes his position clear:

(1) The typical embryos of the Pteridophytes and Angiosperms
differentiate into three primary members, the cotyledon, stem, and
root ; (2) cotyledons are not arrested leaves, but are primarily hausto-
rial organs originating phylogenetically as the nursing-foot in the
Bryophytes and persisting throughout the higher plants; (3) the mono-
cotyledonous condition is the primitive one and prevails in the Bryo-
phytes, Pteridophytes, Monocotyledons, and some Gymnosperms; the
two (sometimes more) cotyledons of the Dicotyledons are jointly the
homologue of the single cotyledon of the Monocotyledons ; (4) the
cotyledon always occurs at the base of the primary stem; (5) the hypo-
cotyl is a structure peculiar to the Angiosperms, being differentiated
between the primary stem and root; (6) the so-called cotyledon of
the Pteridophytes and Gymnosperms, with the probable exception cf
Ginkgo and the Cyeads, are true foliage leaves,

THE EMBRYO 209

The same general idea has been expressed by Balfour,®® as
the following quotations show:

“We ought, I think, to look upon the embryo as a protocorm of
embryonic tissue adapted to a seed-life. Under the influence of its
heterotrophic nutrition and seed-environment it may develop organs
not represented in the adult plant as we see in, for instance, the embry-
onal intraovular and extraovular haustoria it often possesses. There
is no reason to assume that there must be homologies between the
protocorm and the adult outside an axial part with its polarity. There
may be homologous organs; but neither in ontogeny nor in phylogeny
is there sufficient evidence to show that the parts of the embryo are a
reduction of those of the adult.”

“That the cotyledons, primarily suctorial organs, should change
their function and become leaf-like under the new conditions after
germination is no more peculiar than that the hypocotyl should take
the form of an epicotylar internode, from which it is intrinsically
different as the frequent development upon it of hypocotylar buds
throughout its extent shows.”

“The protocorm has, I believe, developed along different lines in
the Dicotyledons and Monocotyledons. This has been to the adyan-
tage of the former in the provision that has been made for rapid as
opposed to sluggish further development. Confining ourselves to the
general case, the axial portion of the protocorm of the Dicotyledon,
the hypocotyl, bears a pair of lateral outgrowths, the cotyledons, and
terminates in the plumular bud and in the primary root respectively.
The cotyledons are its suctorial organs, and the hypocotyl does the
work of rupturing the seed and placing the plumular bud and root by
a rapid elongation which commonly brings the plumular bud above
ground, protected, it may be, by the cotyledons. These latter may
then become the first assimilating organs unlike or like to the epico-
tylar leaves. In the Monocotyledons the axial portion of the proto-
corm has usually no suctorial outgrowths. Its apex and usually its
base also are of limited growth. The plumular bud is a lateral devel-
opment, and the primary root often an internal one. The suctorial
function is performed by the apex of the protocorm, termed here also
the cotyledon.”

“T use the term purely as an objective designation, and in the
original meaning of the suctorial organ in the embryo. This terminal
cotyledon in the Monocotyledons is not a leaf nor the homologue of
the lateral cotyledons in the Dicotyledons.”

An explanation of the terminal cotyledon of Monocotyledons
has been suggested by Miss Sargant *® in her study of the seed-
lings of Liliaceae. In Anemarrhena she finds the cotyledon

210 MORPHOLOGY OF ANGIOSPERMS

traversed by two opposed vascular bundles, which suggest the
fusion of two organs and a derivation from the dicotyledonous
condition. This position is further strengthened by the well-
known tendency among certain Dicotyledons for the cotyledons
to become more or less completely fused (see Chapter XV).

The whole problem, however, is too indefinite as yet, and
the data are too few to permit well-grounded conclusions, but it
is well worth consideration.

PARTHENOGENESIS

The term parthenogenesis was once very loosely applied,
ine.uding all cases of the appearance of embryos without fer-
tilization. Strictly, however, it includes only those cases in
which the normal egg produces an embryo without fertilization,
and this phenomenon has thus far been demonstrated in only
three angiospermous genera, to be described below. Apogamy,
being the production of a sporophyte by a gametophyte without
the act of fertilization, of course includes parthenogenesis, but
the production of sporophytes by gametophytic structures
other than the egg may for convenience be distinguished as
vegetative apogamy. In this category would be included all
cases of embryos derived from unfertilized synergids, antip-
odals, and endosperm, the last-named structure being included
or not dependent upon one’s view as to its morphological char-
acter. When an unfertilized synergid produces an embryo, it
nught be claimed that it is not a case of vegetative apogamy
but of parthenogenesis, since the synergid is to be regarded as a
non-functioning egg. This simply serves to illustrate the fact
that categories are essentially arbitrary and artificial. A third
eategory includes those cases in which embryos are produced by
the tissue of the nucellus or of the integument. This is not
apogamy, although it has often been so called, for it is a ease in
which a sporophyte is produced by sporophytie tissue, and ean
be included under the general name of budding. In addition
to the normal method, therefore, embryos appear among Angio-
sperms in three ways, namely, by parthenogenesis, by vegetative
apogamy, and by budding. In most eases vegetative apogamy
and budding are associated with polvembryony, and they will
be considered under that head. The three well-authenticated
eases of parthenogenesis among Angiosperms are as follows:

THE EMBRYO 211

In 1898 Juel ** °° reported parthenogenesis in Antennaria
alpina, and two years later published a very full account of
this species and also of A. dioica, in the latter of which fertili-
zation occurs regularly. In the parthenogenetic A. alpina usu-
ally only pistillate plants are found, and in the staminate plants
that do oceur the pollen is either lacking or feebly developed.
Juel was able to show conclusively that the embryo develops
from the unfertilized egg. He was also able to satisfy himself
that the number of chromosomes (about fifty) remains un-
changed throughout the entire life history, no reduction taking
place in the formation or germination of the megaspore. The
first division of the nucleus of the megaspore mother-cell is like
the divisions in vegetative cells, and neither in the form of
chromosomes nor in the character of the spindle does it resemble
the heterotypic division that is so constantly associated with the
reduction of chromosomes. The mother-cell gives rise to only
one megaspore, not forming a tetrad. In A. dioica, in which
fertilization regularly occurs, the megaspore mother-cell gives
rise to a tetrad, the first division being accompanied by a reduc-
tion in the number of chromosomes (from about twenty-four to
about twelve). While the number of chromosomes was not de-
termined with absolute accuracy for either species, the numer-
ous countings prove the principal point, namely, that in A.
dioica a veduction occurs at the beginning of the gametophyte
generation, but in the parthenogenetic A. alpina the number
remains neh en aed throughout the life history. In the latter
also the polar nuclei do not fuse to form a primary endosperm
nucleus, but each divides independently and forms a mass of
endosperm, showing, like the egg, an ability to divide without
previous fusion.

In 1901 Murbeck 7° discovered that parthenogenesis is more
or less constant in all the species of Alchemilla belonging to
Evatcuremitia; but he succeeded in finding a species (A. ar-
vensis) in which fertilization regularly occurs. In the struc-
ture of the nucellus Alchemilla differs decidedly from Anten-
naria, there being a large number of megaspore mother-cells,
many of which form tetrads; and it is not uncommon for sey-
eral of the resulting megaspores to germinate. The general
appearance of the eribeye: -sac is normal, and the polar nuclei
usually fuse to form a primary endosperm nucleus. Since this

212 MORPHOLOGY OF ANGIOSPERMS

fusion was observed in several parthenogenetic species of Al-
chemilla (A. sericata, A. “ hybrida,’ A. pubescens, A. pasto-
ralis, A. acutangula, A. alpestris, and A. speciosa), its failure,
as in Antennaria alpina, can hardly be regarded as character-
istic of parthenogenetic forms. In the parthenogenetic species
of Alchemilla, as Antennaria alpina, the number of chromo-
somes remains unchanged throughout the life-history. Al-
though the number was not positively established, the counting
never showed less than thirty-two or more than forty-eight.
In Alchemilla arvensis, in which fertilization regularly oecurs,
the numbers are sixteen and thirty-two. Aside from the more
difficult cytological evidence, a convincing proot of the existence
of parthenogenesis in -l/chemilla alpina is found in the facet
that the segmenting embryos are often obtained from unopened
buds in which no pollen has been developed. In A. arvensis
(Murbeck *), in which fertilization occurs, the pollen-tube en-
ters the chalaza and traverses the integument.

In 1902 Overton ** discovered parthenogenesis in Thalic-
rens, the investigation having been suggested by

trum purpuras t
an early observation that Thalictrum Fendleri set seed freely
in the absence of staminate plants. Only ovulate plants were
brought into the greenhouse and forced. These set seed con-
taining good embryos several weeks before the staminate plants
of the vicinity had developed pollen. Investigation showed
bevond a peradventure that these embryos were derived from
unfertilized eggs. He also compared normal and parthenoge-

e

netic embryos, and found that the latter are noticeably slower
in starting, though the two kinds become exactly alike at matu-
rity. The eytoplasin is very dense about the unfertilized ege,
and when a zone in contact with the ege changes in appear-
ance the first segmentation oceurs. He suggests that there is
a reaction of some kind between the egg and the contiguous
eytoplasim that brings about the change in the physical eon-
stitution of the ege that induces segmentation. This is con-
eeivable from the fact that artificial parthenogenesis has been
induced in the unfertilized eges of certain low animals by
changing the osmotie pressure. Overton finds that in nature
this species probably produces normal and parthenogenetic em-
bryos in about equal munbers.

Still more recently Treub *? has concluded that Ficus hirta

THE EMBRYO 213

produces parthenogenetic embryos. The observation was not
direct or conclusive, the inference being based upon the failure
to discover pollen-tubes although embryos were common, the
feeble development of endosperm, and the poorly developed
synergids, all of which is negative evidence. Treub suggests
that the stimulus that induces the egg to divide in this case
is the puncture made by the pollinating wasp Blastophaga.

There seems to be no doubt that other cases of partheno-
genesis will be discovered among Angiosperms, and that many
embryos supposed to be normal are parthenogenetic. There
seems to be no reason to doubt that if an envelop of cytoplasm
may result in the segmentation of the ege in Thalictrum, it may
often have the same result in other cases. For example,
Treub *° observed that in certain Burmanniaceae (Gonyanthes
candida and Burmannia javanica) the ege does not segment
until the embryo-sae is packed full of endosperm. Such a con-
dition might well repeat the results in Thalictrum. In fact,
all cases in which there is a long delay before the egg segments
may be suspected of occasional parthenogenesis.

POLYEMBRYONY

Polyembrvony in Angiosperms, while not so prevalent as in
Gymnosperms, is by no means a rare or recently discovered
phenomenon. As early as 1719, Leeuwenhoek found two em-
bryos in orange seeds. In Huonymous latifolius polyembryony
was discovered three times independently; by Petit-Thouars in
1807, by Grebel in 1820, and by Treviranus in 1838. In this
species about one-half of the ripe seeds are said to contain more
than one embryo. A. Braun in 1859 gave an historical resumé
of the subject, and cited sixty cases as known at that time.
The first demonstration of the real nature of certain cases of
polyembryony was made by Strasburger’* 1° in 1878. THe
found that in Funkia ovata, Nothoscordon fragrans, Citrus
Aurantium, and Coelebogyne ilicifolia the cells of the nucellus
above the apex of the embryo-sac become rich in contents, divide
and grow, and form several embryos that push the sac wall
before them and become placed in the seed like normal em-
bryos. In Funkia the egg is fertilized, but seldom or perhaps
never produces an embryo, dividing a few times and then disor-
ganizing (Fig. 99). When pollination is prevented artificially,

214 MORPHOLOGY OF ANGIOSPERMS

the adventitious embryos begin to develop but never mature. In
Cilrus the embryos are derived not only from the cells of the
nucellus capping
the sac, but also
from those lower
down, which may
be separated from
the sac by several
cells. In Coele-
bogyne, long sup-
posed to be par-
thenogenetic, fer-
tilization never

occurs in Europe,
Fre. 99.—Funkia ovata, showing adventitious embryos ; fer-
tilized egg has given rise to weak proembryo of three
eclls; x 190.—After SpRAsSBURGER.1e ate plants are
cultivated. These

are not eases of apogamy, as often stated, but are evidently

since only pistil-

cases of vegetative multiplication or budding, since the em-
bryos arise from sporophytic tissue. In Opuntia vulgaris
(Ganong *) the ripe seed contains one large embryo and sev-
eral smaller ones pressed to one side. Talf ripe seeds generally
show that the large embryo comes from the micropylar end of
the sac, while the small ones arise from nucellar tissue. Among
Cactaceae the only previously
known case of polyembrvony is
that of Opuntia tortispina.

The multipheation of em-
bryos by budding from a imass-
ive suspensor also oceurs, and
is especially common in the
Lilium type of embryogeny, in
which the suspensor is strongly
meristematic. In 1895 Jef-
frey *° called attention to the
fact that in Brythrontum ameri- Fre. 100. — Erythronium americanum.

canwmn the suspensor is a mass- Four embryos derived from fertilized
F i egg; x 144.—After Jerrrey.3

ive and lobed tissue on whose

free surface two to four embryos appear, only one persisting

(Fig. 100). As in Funhkia, the eels of the nucellus are

THE EMBRYO 215

rich in protoplasmic contents, and this led Jeffrey to sus-
pect that a reinvestigation of Funkia with the aid of modern
technique would reveal a similar condition. The examination,
however, confirmed Strasburger’s account, so that while the
general appearance of sections is much the same in the two
vases (cf. Figs. 99 and 100), it is established that in Punkia
the embryos come from the nucellus, while in Hrythronium they
come from the fertilized egg. In Erythronium albidum Schatt-

Fie. 101.—Limnocharis emarginata. A-C, three sections of one embryo, showing em-
bryo proper (e) and embryo-buds from suspensor (em); D, appearance of growing

point of stem (gp).—Atter Hav.

ner 72 found the same large, irregular, and much-lobed sus-
pensor, but it was associated with only one embryo. In Tulipa
Gesneriana Ernst * also observed the phenomenon of a massive
suspensor associated with one to six embryos, only one of which
usually persists. In these cases the Lilium type of embryogeny
is obscured by the early and rapid growth of the suspensor
region of the proembryo, the embryonal cell appearing hardly
more than one of the cells of its free surface. In these cases

15

216 MORPHOLOGY OF ANGIOSPERMS

of polyembryony, therefore, one of the embryos is to be regard-
ed as normal, and the others as secondary or adventitious. Ex-
actly the same thing sometimes occurs in Limnocharis emargr
nata, one of the Alismaceae, as observed by Hall ** (Fig. 101).
In this species the basal suspensor-cell may
increase very much in size and remain un-
divided, as is most common in the Alisma
type; or it may divide extensively, forming
a massive tissue from which several embryos
bud. It was not observed whether more
Fic. 102.—-Mimosa Den. than one embryo matures, but presumably

hartii. Threeembryos not. This case is interesting not only on
occupying position of

Lecartates MSE account of the polyembryony, but also be-
— After Guienarp.2. Cause it emphasizes the relation between the
Alisma and Lilium types of embrvogeny.

Illustrations of ordinary apogamy are relatively numerous,
apparently every cell within the embryo-sac being able under
certain conditions to produce an embryo. In some cases a
synergid is fertilized, and then the resulting embryo should
probably be regarded as normal; it certainly is not apogamous.
For example, Schwere *° discovered
svnergid fertilization in Tararacum
officinale; and Guignard * has ob-
served that in Natas major the per-
sistent synergid instead of the pri-
mary endosperm nucleus may be fer-
tilized by the second male nucleus,
resulting in two embryos lying side
by side (Fig. 103). An embryo from
a synergid in addition to a normal Fie. 103.—Naias major. Two

embryo from the eee has been re- embryos, one from fertilized
: es : egg, the other from fertilized
ported by several observers. In J/7- cenit, Aangtouucleds Ene

mosa Denhartit Guignard 71 has found ing fused with nucleus of
eases which suggest the development synergid instead of polar nu-

. cleus; e, endosperm nucleus;
of embryos from all three cells of the

: x 176.—After Gvien arp.
ege-apparatus. Sometimes two simi-

lar embryos appear, one in the position of the ege and the

: ) a
other in that of @ synereid; sometimes a group occurred con-
— ‘

sisting of one im@hanged synergid, one embryo in the egg
position, and a second embryo in the position of the seeond

THE EMBRYO 917

synergid; and in one case three embryos were seen occupying
the position of the egg-apparatus (Fig. 102). Although favor-
ing this interpretation, Guignard mentions the possibility that
the extra embryos may have come from the separation of early
segments of the egg, a view doubtless suggested by the separa-
tion of the cells of the suspensor in certain of the Legu-
minosae.

In Vincetoxicum nigrum and V. medium Chauveand *3
finds that polyembryony is a regular phenomenon, one, two,
three, four, and even five embryos appearing, more than one
of which may reach maturity. The synergids are doubtless
involved. Chauveaud found four or five bodies in the pollen-
tube which he thought might be interpreted as male nuclei, and
responsible for polyembryony. He also concludes that poly-
embryony is a primitive feature of Angiosperms, the number
having been reduced in the interest of one strong embryo. In
describing synergid fertilization in Iris stbirica, Dodel*? im-
plies a somewhat similar view, when he interprets the synergids
as partially aborted eggs. In this form more than one pollen-
tube may enter the micropyle.

In certain orchids, as Gymnadenia conopsea (Stras-
burger 1°), two embryos sometime occur in the same sac, but
their origin is uncertain, although it is very probable that one
of them is derived from a synergid, either apogamously or by
fertilization.

In a preliminary paper, Hegelmaier ™ states that polyem-
bryony is habitual in Buphorbia dulcis, two to nine embryos
appearing at the micropylar end of the sac. One of the em-
bryos, which certainly comes from the egg and may be dis-
tinguished from the others by the presence of a suspensor,
becomes the functional embryo. Fertilization was not studied,
and so the origin of some of the embryos is in doubt, although
it is certain that some come from the nucellus. Two embryos
often reach the cotyledon stage, with tissue systems differen-
tiated, while the others appear as irregular masses.

Allium odorum presents a remarkable case of polyembryony.
In 1895 Tretjakow *® reported one to three embryos from the
antipodal cells (Fig. 104), the fertilized egg and sometimes a
synergid forming additional embryos. In the same species

Hegelmaier ** observed five embryos in a single embryo-sac ;

218 MORPHOLOGY OF ANGIOSPERMS

one normal, one from a synergid, two from antipodal cells, and
one from the inner integument (Fig. 105). It is interesting
to note that while polyembryony is so frequent in Allium odo-
rum, it has not been observed in other
species of the genus. Hegelmaier exain-
ined A. fistulosum and A. ursinwn, and
Elmore °° made a thorough study of A,
cernuum, A. tricoceum, and A. canadense,
without discovering a single extra em-
bryo, reporting also very small and eva-
nescent antipodals. In parthenogenetic
species of Alehemilla Marbeck *° found
embrvos from the egg, from the synergids,

Fie. 104.— Allium odorum.
Three embryos derived ‘ 4
from the threé amtipe- arid fron the nucellar tissue (Pig. 106).
dal sells: L1G attr In Balanophora elongata and B. glo-

ora bosa fertilization is known not to oceur,

and both Treub 4% and Lotsy *8 state that the embryo is formed
by the upper polar nucleus. In addition to this, a cell in the
midst of the endosperm is said to develop imto a five to ten-
celled “ pseud-embryo,” whose significance and history we are

A

Fie. 105.— Allium odorum. A, section of ovule with four embryos, one from egg, one
from a synergid, ore from an antipodal cell, and one from the wall: 15; B, two
embryos, one from egg and one from a synergid; the other synergid somewhat
enlarged and lying between the two embryos; x 246; C,embryo derived from inner
integument: 7, inner integument; 0, outer integument; x 246.—Atter HEGEL MAIER.%

at a loss to understand (Fig. 107). In the allied /Telosis quaya-
nensis, also, Chodat and Bernard © think that fertilization does
not oceur, and that the embryo arises apogamously from the
endosperm,

Tt is evident that polyembryony is by no means so rare a

THE EMBRYO 219

phenomenon as many may have supposed. The cases on record
are already so numerous that only an exhaustive study of the
literature would make it safe to venture an estimate of the
number, Since in nearly all the cases described this phenome-
non 1s rare rather than habitual, it is probable that wnder con-
ditions not yet understood a large number of plants may exhibit
polyembryony occasionally.

Fic. 106.—Embryos in parthenogenetic species of Alehemilla. A, A. sericata, one par-
thenogenetic embryo from egg and one from synergid, the other synergid breaking
down; the two polar nuclei and antipodal cells also shown; x 284; DB, A. pastoralis,
showing one synergid partly disorganized, one embryo of four cells from unfertilized
egy, one embryo from nucellus, two polar nuclei and one synergid nucleus forming
group at middle of sac, also three disorganizing antipodal cells; x 190. After
Murzeck.®

The scattered literature of the subject is admirably sum-
marized by Ernst ° in his presentation of polyembryony in
Tulipa Gesneriana. The following synoptical statement is
taken from Ernst, and supplemented by the more recent addi-
tions. In case the same form is treated in several accounts,
there is no attempt to cite all of them or even the first refer-
ence, but a selection is made of those citations that direct to

Fie. 107.—Balanophora elongata. Stages in development of embryo-sac, endosperm,
and embryo. A, archegonium-like megasporangium with mother-cell that becomes
megaspore directly without forming tetrad; x 145; 2B, quadrinucleate stage of
embryo-sac ; x 200; C, nearly mature sac showing above the two synergids and
oosphere, just beneath the micropylar polar nucleus, and at opposite end of sac a
group of four nuclei, the three antipodals, and the lower polar nucleus; x 280; D,
at upper eud the synergids and egg are disorganizing, just beneath are two cells
resulting from first division of upper polar nucleus; x 280; £ysix cells of endosperm
shown; synuergids and egy still visible at upper end of sac; x 800; F, two-eelled
embryo formed from an inner cell of the endosperm ; x 300,—After TREuB.4s

220

THE EMBRYO 221

the most complete descriptions. The forms that Ernst includes
under * pseudo-polyembryony ”
sion of the subject.

are not treated in our discus-

Pseudo-polyembryony.

1. OVULES GROWN TOGETHER. Pirus Malus, Loranthus ewro-
paeus, Viscum album (all A. Braun *).

2. Division OF NUCELLUS. Morus albus (Hofmeister*), Orchis
Morio (Braun*), Gymnadenia conopsea (Strasburger™), Coffea ara-
bica (Hanausek *’).

3, DEVELOPMENT OF SEVERAL EMBRYO SacsS IN THE SAME NU-
cELLUS. Cheiranthus Cheiri (Schacht*), Rosa sp. (Hofmeister ?),
Rosa livida (Strasburger *), Trifolium pratense (Jénsson **), Taraxa-
cum officinale (Schwere *").

True Polyembryony.

A. Embryos derived from cells outside the sac, hence from sporo-
phytic tissue (vegetative multiplication or budding).

1. Empryos DERIVED FROM CELLS OF THE NUCELLUS. Funkia
ovata (Strasburger ”), Nothoscordon fragrans (Strasburger™), Citrus
Aurantiuwm (Strasburger "*), Mangifera indica (Strasburger *), Huony-
mus americanus (Braun*), Coelebogyne ilicifolia (Braun,* Stras-
burger), Clusia alba (Goebel), Opuntia vulgaris (Ganong **), Al-
chemilla pastoralis (Murbeck °°).

2. EMBRYOS FROM CELLS OF THE INTEGUMENT. Allium odorum
(Tretjakow,** Hegelmaier **).

B. Embryos derived from cells within the sae (parthenogenesis
and vegetative apogamy) ; although not in the same morphological
category, embryos from the suspensor are also included in the list
(vegetative multiplication or budding).

1, NoRMAL OcCURRENCE OF Two Eacs. Santalum album and
Sinningia Lindleyana (both Strasburger ™).

9. Empryos FROM SyneRGIDs. Glaucium lutewn (Hegelmaier”),
Mimosa Denhartii and Schrankia uncinata (Guignard*), Iris sibi-
rica (Dodel®), Lilium Martagon (Overton), Vincetoxieum nigrum
and V. medium (Chauveaud *), Alliam odorwm (Tretjakow,” Hegel-
maier®), Taraxacum officinale (Schwere*’), Aconitum Napellus
(Osterwalder®), Alchemilla sericata (Murbeck"), Naias major
(Guignard ”).

8. SPLITTING OF EMBRYO DERIVED FROM Ecce. Loranthus euro-
paeus (Braun *).

4. Empryos FRoM ANTIPODAL CELLS. Allium odorum (Tretja-
kow,** Hegelmaier *’).

5. Empryos FROM ENDOSPERM CELLS. Balanophora elongata
(Treub *°).

222

MORPHOLOGY OF ANGIOSPERMS

6. EMBRYOS FROM THE Suspensor. Hrythronium dens-Canis
(Hofmeister®), HE. americanune (Jettrey ), Tulipa Geswerictiiat
(Ernst), Limnocharis emarginata (Hall *).

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S4. STRASBURGER, E. Ein Beitrag zur Kenntniss von Ceratophylluim

submersum und phylogenetische Erérterungen. Jaliarb. Wiss.
Bot. 87: 477-526. pls. 9-11. 1902.

5. Ltoyp, F. E. The Comparative Embryology of the Rubiaceae.

Mem. Torr. Bot. Club 8: 27-112. pls. 5-15, 1902.

86. Jounson, D.S. On the Development of Certain Piperaceae. Bot.

Gazette 84: 321-340. pls. 9-10, 1902.

. Pkcnoutre, F. Contribution a l’étude du développement de

Vovule et de le graine des Rosacées. Ann. Sci. Nat. Bot. VIII.
16: 1-158. figs. 166. 1902.

. Lyon, H. L. The Phylogeny of the Cotyledon. Postelsia 1901:

55-86, 1902.

89. SARGANT, ETHEL. The Origin of the Seed-leaf in Monocotyledons.

The New Phytologist 1: 107-113. pl. 2. 1902.

0, MURBECK,S. Ueber Anomalien im Baue des Nucellus und des

Embryosackes bei parthenogenetischen Arten der Gattung Al-
chemilla. Lunds Univ. Arsskrift 88%: no. 2. pp. 10. pls. 1.
1902,

. Scumip, B. Beitriige zur Embryo-Entwickelung einiger Dicotylen.

Bot. Zeit. 60: 207-230, pls. 8-10, 1902.

. TrEevB, M. L’organe femelle et lembryogénése dans le Ficus

hirta Vahl. Ann, Jard. Bot. Buitenzorg II. 8: 124-157. pls. 10-
25. 1902.

. JueL, H. 0. Zur Entwicklungsgeschichte des Samens von Cyno-

morium. Beih. Bot. Centralbl. 13: 194-202. figs. 5. 1902,

SARGANT, ErHeL. A Theory of the Origin of Monocotyledons,
founded on the Structure of their Seedlings. Annals of Botany
17: 1-92. pls, 1-7, 1908,

5. Murpeck, 8. Ueber die Embryologie von Ruppia rostelata

Koch. Handl. Svensk. Vetensk. Akad. 36: pp. 21. pls. 3. 1902,

CHAPTER X
CLASSIFICATION OF MONOCOTYLEDONS

A satisractory classification of Angiosperms stil] remains
an linpossible task. The immense number of species and their
entanglement of relationships, as well as our merely superficial
knowledge of the great majority of forms, have made progress
toward a natural classification very slow. Since the time of
John Ray (1703) steps in this progress have been taken by
De Jussieu (1789), De Candolle (1819), Endlicher (1836-
1540), Brongniart (1543), Braun (1864), Bentham and
Hooker (1862-1883), Eichler (1883), Engler (1892), and
others. Naturally, the increasing knowledge of morphology
and the changed conception of species have gradually broken
up artificial assemblages, but much of classification is still arti-
ficial. It does not He within the purpose of this book to trace
the historical development of classification, nor to present an-
other scheme for consideration. We merely adopt the classi
fication of Eichler as modified by Engler, and elaborated in
Engler and Prantl’s Die Nattirlichen Pflanzenfamilien, as the
best expression of our present knowledge of morphology as
applied to the whole of Angiosperms. The special student of

morphology must have enough knowledge of general relation-
ships to enable him to select critical forms for investigation and
to appreciate the bearings of his results. The purpose of the
following presentation,- therefore, is to trace in a general way
the evolution of Angiosperms and to point out the greatest gaps
in knowledge, using the classification mentioned as the best
available basis. No attempt is made to use the varying termi-
nology of the larger groups of classification, but coordinate
groups are indicated by comimon endings.

According to Engler, the general tendency among Monocot-

9907

and

228 MORPHOLOGY OF ANGIOSPERMS

arranged and indefinite in number to pentacyclic trimerous
flowers. There are also such lines of advance as from apocarpy
to synearpy, from hypogyny to epigyny, from actinomorphy
to zygomorphy, ete. These tendencies are often very unequally
expressed even by different groups of the same allance, one
eroup developing chiefly along one lune, and another group
along another line, so that the results are very different. It is
also often a question whether a simple floral structure is primi-
tive or reduced. In the older morphology there was a typical
floral structure, and all simpler ones were regarded as reduced
forms. There can be no doubt that there are reduced floral
structures, as in Lemna; but the great majority of simple
flowers are probably primitive.

Upon these and other considerations, Engler has subdivided
the Monocotyledons into ten great alliances. The first six con-
stitute the more primitive Spiral series, and although the trim-
erous habit appears among them, the spiral arrangement and

yledons is to advance from naked flowers with parts spirally

indefinite numbers occur in one or more sets. The remaining
four alliances constitute the Cyclic series, the highly specialized
Monocotyledons.

I. Panpanatrs.—This includes the Pandanaceae, Typha-
ceae, and iia uate together containing a little more than
100 species. The Pandanaceae (about SO species), or serew-
pines, belong to the oriental tropics, chiefly the coasts and is-
lands of the Indian and Pacifie oceans; while the other families
are mainly represented in temperate regions.

That these forms are primitive Monocotyledons is indicated
by the following facts: there is nothing to represent a perianth
unless the floral bracts of Sparganium he regarded as one: the
sporophylls are mostly spiral and indefinite in number, the sta-
mens of Pandanaceae often being very numerous and exhibiting
the greatest variation in arrangement; the species are all hydro-
phytic; and the plants are anemophilous. Such flowers as those
of the Pandanaceae and Typhaceae are extremely simple, the
peeuhar hairs accompanying the sporophylls of the latter ap-
i tly representing sterile sporophylls; while the Spargania-

rae are the most advaneed members of the alliance, a perianth
ae heing represented by a set of small bracts, and the
trimerous character appearing.

CLASSIFICATION OF MONOCOTYLEDONS 229

A well-marked feature of the group is the protection of the
flower-clusters by a prominent leaf-sheath. The development
of this sheath as a protecting organ before the appearance of a
fully developed perianth is one of the constant features of the
more primitive Monocotyledons, and in some of the following
groups it becomes highly specialized.

The hydrophytic Pandanales, therefore, begin in the great-
est simplicity, so far as floral structures are concerned, the
Pandanaceae being the most primitive forms on account of the
indefinite number of the sporophylls and the spiral arrangement
of the stamens, and the series has not advanced very far. It
should be remembered, however, that the three existing families
probably represent fragments of a formerly much larger alli-
ance, so that the association of the temperate Typha and Spar-
ganium with the tropical Pandanaceae may not be so unnatural
in reality as it appears at present. It is. extremely desirable to
obtain some accurate knowledge of the essential morphology of
the Pandanaceae.

Tl. Herosrares.—This includes the Potamogetonaceae,
Naiadaceae, Aponogetonaceae, Juncaginaceae, Alismaceae, Bu-
tomaceae, and Hydrocharitaceae, together containing about 235
species. Engler has set apart the small family Triuridaceae,
containing about 18 species, as representing a distinct series,
Trivripsres, but this can be disregarded in this very general
presentation.

This is one of the most remarkable of the monocotyledonous
lines in its extent, reaching trom the greatest floral simplicity
in Potamogetonaceae to highly developed flowers in Hydro-
charitaceae. It has been called an unstable or plastic line, and
may have given rise to higher forms; in any event it is probably
to be regarded as one of the most important phylogenetic lines
among the Monocotyledons. For this reason morphological
investigation in recent years has specially cultivated this series
of forms, particularly the more primitive families. About the
only taxonomic character that holds these diverse forms together
is the fact that they are exceptional among Monocotyledons in
the fechle development of endosperm. They are characteris-
tically aquatic, and sheathing bracts enclosing the flower-clus-
ters are largely developed. In most of the forms the spiral
arrangement and indefinite number of floral parts is very appar-

230 MORPHOLOGY OF ANGIOSPERMS

ent, but the line as a whole presents almost a complete series
from the simplest floral structure to one of the most highly
developed.

The series of floral changes may be broadly indicated as
follows. In Potamogetonaceae and Naiadaceae there is no peri-
anth, and the stamens and carpels are indefinite in number; in
Juncavinaceae a bract-like perianth is present, there is a dis-
tinct tendency toward the trimerous habit, and syncarpy may
occur; in Alismaceae the perianth is differentiated into calyx
and corolla, and the trimerous tendency is very clear, though
the carpels are usually indefinite in number; in Hydrocharita-
ceae, in addition to a differentiated perianth and a strong ex-
pression of the trimerous tendency (although the stamens and
earpels are often indefinite in number), the flowers are epigy-
nous. The plants are chiefly anemophilous or hydrophilous,
but the appearance of a differentiated perianth in the Alisma-
ceae is probably associated with a certain amount of ento-
moph 1 ly.

Heliobales, therefore, begin with as great simplicity of
floral structure as do the Pandanales, but they have advanced
much further in floral development. That such an extensive
line comprises so few species is probably associated with the
uniformity of aquatie conditions. In the whole series, how-
ever, there is no distinct settling into a complete trimerous
habit, which is intimated rather than established.

TIL. Grumares.*—In this alliance are the two great fami-
lies Gramineae and Cyperaceae, the former including about
351 wenera and 4,700 species, the latter 76 genera and about
2,300 species. In point of species this is one of the greatest of
angiospermous alliances, and in display of individuals it is un-
questionably the greatest. The common features of the two
families ave the absence of a perianth, the protection of the
flowers by special bracts, the Huctuating of the stamens between
one and many, the solitary carpel, and anemophily. It is not
probable that the two families are related to one another genet-
ically, but they represent approximately the same stage of floral
development.

The peenhar features of the bract-proteetion, as contrasted

* GLUMIFLORAE of Engler.

CLASSIFICATION OF MONOCOTYLEDONS 231

with the preceding alliances, is that the bract does not ensheath
a whole flower-cluster but individual flowers. It is this charac
teristic bract (glume, palet) that gives name to the alliance.
The lodicules of Gramineae and certain hairs and bracts of
Cyperaceae are regarded by some as representing a perianth.
Even if this doubtful claim be allowed, such a perianth is
better regarded as one that is very primitive rather than re-
duced.

The primitive character of Glumales is indicated by the
characters given above, but contrasted with the Helobiales it is
a rigid group that has not advanced far in floral development,
but has proved to be a remarkably successful type of vegeta-
tion. Moreover, it is the primitive group of Monocotyledons
that seems to have been the first to establish itself upon the
drier and more diversified land surface, and this fact may hold
some relation to its structural stability and its great display of
species. Evidence of its aquatic origin may be obtained not
only from the numerous hydrophytic forms, but also from ana-
tomical characters that relate it to Helobiales and Pandanales
rather than to the terrestrial alliances.

Pandanales, Helobiales, and Glumales are the only three
alliances of Monocotyledons that include the most primitive
type of monocotyledonous floral strueture. Their possible ge-
netic relation to one another is entirely obscure, and in their
present display they seem to emerge from the beginnings of the
history of Monocotyledons as independent lines. The remain-
ing seven alliances are either derived from these three, or their
primitive members have disappeared.

IV. Patmares.*—The palms are the chief representatives
of monocotyledonous trees, and are characteristic of all tropical
regions. The single family Palmaceae includes about 150 gen-
era and 1,100 species, though these numbers will doubtless be
much increased when the palms are studied in their habitats.
A knowledge of the essential morphology of this group is also
much to be desired.

A perianth is always present, although it is very “ rudimen-
tary” and hence doubtful in Phytelephas and Coryphanthe,
but it is not differentiated into a distinct calyx and corolla.

* Principes of Engler.
16

232 MORPHOLOGY OF ANGIOSPERMS

As there are no naked flowers, this group does not have as
primitive members as do the three preceding ones. The sta-
mens are extremely variable in number, ranging from three
to indefinitely numerous, showing the primitive spiral charac-
ter; while the carpels are usually three and sometimes form a
synearpous pistil. The enormous flower-cluster is ensheathed
by a great bract (spathe) that is more or less tough and even
woody, a feature recalling the same tendeney in Pandanales
and Helobiales. As the axis of inflorescence is sometimes
thickened and the flowers more or less embedded in it, the
inflorescence is often spoken of as a branching spadix.

These characters indicate a group as a whole considerably
further advanced than the preceding ones in the constant pres-
ence of a definite perianth, although it is undifferentiated. The
association of floral envelops with a spathe is of interest, but
in such conditions a highly developed perianth could not be
expected. While there is doubtless anemophilous pollination,
entomophily must exist to a certain extent. The whole struc-
ture suggests one that is intermediate between the dominance
of bract and perianth, between anemophily and entomophily.

Palnales, therefore, differ from Glumales in the definite
trimerous perianth, as well as in numerous other features;
from the Helobiales in that the number of carpels is constant ;
but through Phytelephas and Coryphanthe, with their rudimen-
tary perianth, as well as through general habit, the connection
with Pandanales seems clear. It seems probable, therefore,
that the Palmales have been derived from the Pandanales, sur-
passing the Glumales in floral development, but not reaching
the differentiation of calyx and corolla and epigvny attained by
the higher members of the THelobiales.

V. Syxanruares.*—This includes a small family (Cy-
clanthaceae) of the American tropics, represented by about 45
species, and usually and naturally associated with the serew-
pines and palms. The flowers are in an unbranched spadix,
either seattered or in a close spiral, and there is generally an
evident bract-like perianth in one or two eveles. The stamens
range from six to indefinitely numerons, and the carpels are
one to four. In the staminate flowers there is no trace of ear-

* SYNANTHAE of Engler.

CLASSIFICATION OF MONOCOTYLEDONS 233

pels and the stamens are connate; while in the carpellate flowers
there are very conspicuous and often branching staminodia.
There is a strong tendency to * :

“

coalescence ” in all the members,
the perianth often being tubular, the stamens usually connate,
and the carpels (if more than one) always forming a syncar-
pous pistil. The group is also peculiar in the very numerous
ovules upon a single parietal placenta.

Too little is known of the morphology of the group to speak
of its relationships with any definiteness, but it seems safe to
regard it as another branch of the Pandanales stock. The Pan-
danales, Palmales, and Synanthales are thus referred to a com-
mon origin, with the Pandanales as the most primitive repre-
sentative of the stock. This tropical association seems to be a
strange one for Typha and Sparganium, but otherwise it seems
to be entirely natural, and not clearly related to any other Mono-
cotyledons.

VI. Araves.*—This includes the Araceae with about 1,000
species, and the Lemnaceae with about 25. The Aroids form
one of the most distinct and also diversified groups of Monocot-
yledons. The characteristic features are the spadix, the highly
developed spathe, and the broad net-veined leaves. There is
also probably greater anatomical differentiation than in any
other monocotyledonous group, which is taken advantage of
in their classification. The floral structure is of three general
types: (1) the Calamus type, in which the flowers are bisporan-
giate, pentacyclic, 2 to 4-merous, and synearpous; (2) the Calla
type, in which the flowers are bisporangiate, with no perianth,
6 to 9 stamens, and 1 carpel; (5) the Arum type, in which
the flowers are monosporangiate (staminate flowers above and
carpellate flowers below on the same spadix), and with no
perianth.

It is evident that the floral structure is extremely fluctua-
ting, and that this is probably associated with the extreme spe-
cialization of the spathe. Engler has called attention to the
fact that the flowers with a perianth are associated with a
bract-like spathe; while those without a perianth (the great
majority) are associated with a petaloideous spathe. In any
event, the bract reaches its highest specialization in this group,

* SPATHIFLORAE of Engler.

204 MORPHOLOGY OF ANGIOSPERMS

being not merely a protecting organ, but immensely varied in
form, texture, and color to secure entomophily. In other words,
the conspicuous function of the perianth in the petaloideous
groups is here assumed by the spathe, and the flowers retain
for the most part the primitive character.

There are many features of the Aroids that suggest the He-
lobiales, especially the Potamogetonaceae, so that Engler
inclines to the belief that they have been derived from that
stock. If this be true, they represent a strong terrestrial branch
from the aquatic Helobiales, that in tropical conditions has
become extremely varied in form and structure, and that has
assumed.the erect, climbing, and epiphytic habits. It does not
seem probable that any other monocotyledonous alliance is asso-
ciated with these two in origin; but the suggestion has been
made that from the Aroids the Dicotyledons, or at least some
of their phyla, may have been derived. One of the most prom-
ising fields of morphological research is among the tropical
Aroids.

The Lemnaceae represent a distinct reduction series, being
Aroids adapted to the free-swimming habit, and remarkably
reduced in structure, Wolffia being the smallest known seed-
plant.

The six great alliances just considered constitute the Spiral
series of Engler, with inconstant number of floral members,
with mostly no perianth or one not adapted to entomophily,
and with a striking development of sheathing leaves or bracts
in connection with the inflorescence or the individual flowers.

The four remaining alliances constitute the Cyclic series, in
which the almost constant floral formula is perianth 3 + 3
stamens 3 + 8, carpels 3 and forming a synearpous pistil. The
two perianth sets may be variously modified, but there runs
through the series an increasing specialization of the perianth

5

for entomophily, which reaches its extreme expression in the
Orchidaceae. As a consequence, the perianth rather than
bracts becomes the conspicuous floral feature. The pentaey-
che trimerous habit having beeome established, the evclie groups
have largely differentiated in the direction of a conspicuous
perianth, epigyny, and zygomorphy. The number of species
involved is so great that only the broadest outlines can be con-
sidered.

35

bo

CLASSIFICATION OF MONOCOTYLEDONS

VII. Farryares.*—The eleven families of this alliance are
Flagellariaceae, Restionaceae, Centrolepidaceae, Mavacaceae,
Xyridaceae, Eriocaulaceae, Rapateaceae, Bromeliaceae, Com-
melinaceae, Pontederiaceae, and Philydraceae, together contain-
ing a little more than 2,000 species. The large families are
Bromelaceae with over 900 species, Eriocaulaceae with 460,
Commelinaceae with more than 300, and Restionaceae with
nearly 250, The chief character that holds these diverse fami-
lies together and separates them from the Liliales is the thin-
walled endosperm rich in starch, whose cells become easily
broken up and dissociated, resulting in a ‘‘ mealy” or “ crum-
bly ” endosperm.

From the evolutionary standpoint the following facts are of
importance: for the most part the forms are grass-like herbs,
with all habits from aquatie to xerophytic and epiphytic; they
are mostly bracteate forms, the upper bracts showing a decided
tendency to ensheath the inflorescence; they are mostly ane-
mophilous, but some forms have a perianth adapted to ento-
mophily; the perianth ranges from scarious to petaloid, from
undifferentiated to a distinct calyx and corolla, from polypetaly
to sympetaly; the flowers are syncarpous and, with the excep-
tion of a few Bromelias, hypogynous.

Such evidence indicates a relatively primitive cyclie alh-
ance with many characters recalling the spiral forms, the
bract-protection and anemophily not being definitely replaced
by a highly developed perianth and entomophily. The origin
of the series is of course obscure, but the evidence seems to
favor the Glumales as the original stock. As illustrating the
construction of a natural sequence of families, those of this
alliance may be used as follows:

The Flagellariaceae, Restionaceae, and Centrolepidaceae,
belonging to the oriental tropics chiefly of the Southern Hemi-
sphere, have a bracteate undifferentiated perianth and are ane-
mophilous, in habit and general character resembling the Spiral
series.

The Mavacaceae, Xyridaceae, and Eriocaulaceae have a dif-
ferentiated calyx and corolla, and orthotropus ovules with very
small embryos. These three families, together with Restiona-

* Farrnosack of Engler.

236 MORPHOLOGY OF ANGIOSPERMS

ceae and Centrolepidaceae, constitute the main part of the old
group Lnantioblastac, characterized by the orthotropous ovules.

The Rapateaceae, chiefly South American, have a distinct
ealyx and corolla, anatropous ovules, and small embryos.

The Bromeliaceae, the great epiphytic family of the Ameri-
can tropics, have a distinct calyx and corolla, anatropous ovules,
and larger elongated embryos.

The Commelinaceae, in addition to the distinct ealyx and
corolla, show a tendency to zygomorphy. This family has the
orthotropous ovules and small embryos of the Enantioblastae,
but the characters given, as well as the habit and inflorescence,
scem to forbid that alliance.

The Pontederiaceae and the Australasian Philydraceae
have long cylindrical embryos, a general tendency to a reduced
number of stamens and carpels, and in the latter family sym-
petaly.

VII. Litrares.*—The nine families of this alliance are
Juneacene, Stemonaceae, Liliaceae, Haemodoraceae, Aanarylh-
daceae, Velloziaceae, Taccaceae, Dioseoreaceae, and Ividaceae,
together comprising almost 5,000 species. The largest families
are Liliaceae with nearly 2,500 species, Iridaceae with more
than 1,000, and Amaryllidaceae with nearly 900,

This great alliance may be regarded as containing the typ-
ical lighly developed Monocotyledons. It is characterized by

a conspicuous development of the perianth and a prevailing
entomophilous habit. The endosperm cells are thick-walled and
in general contain oil rather than starch, resulting in an endo-
sperm that is not “ mealy,” as in the Farinales. The Junea-
ceae, Hacmodoraceae, and Velloziaceae are exceptions in pro-
ducing a starch-containing endosperm, but the cells do not. be-
come dissociated. In passing from the lower members of the
serics to the higher there is a transition from an unditferenti-
ated scarions perianth to a differentiated and petaloideous one ;
and from hypogyny to epigyny, the four lower families being
hypogynous and the five higher epigynons. .

The sequence of families begins with the Tuncaceae, which
with their grass-like habit, searious perianth, and starchy en-
dosperm, may he fairly regarded as intermediate between Fari-

* LinirLorae of Engler.

CLASSIFICATION OF MONOCOTYLEDONS 237

nales and Liliales. The Liliales are midway in the series, hav-
ing attained a petaloideous perianth and entomophily, and
having become so diversified in structure and habit as to raise
a question as to their monophyletic origin. The Amaryllida-
ceae introduce epigyny, and the highly specialized Iridaceae
complete the series. The last six families are in great need of
morphological investigation in the tropics where they are chiefly
massed.

The genetic connection between Liliales and Farinales
seems clear, so that if the latter are regarded as derived from
the Glumales, the former must be referred to the same stock,
probably dissociating early from the Farinales.

The two remaining alliances are characterized by epigyny
and zygomorphy, highly specialized entomophilous structures,
reduction and modification of stamens, and very small and un-
differentiated embryos. In all probability they are not genet-
ically related, but they resemble one another more than they do
the other alliances.

IX. Scrramryares.*—The four families of this alliance
are Musaceae, Zingiberaceae, Cannaceae, and Marantaceae, to-
gether comprising nearly 800 species, 500 belonging to the
Zingiberaceae. The four families are undoubtedly genetically
related, although the first two are restricted to the oriental
tropics, and the last two to the occidental. In addition to the
characters mentioned above, the replacing of functional sta-
mens by petaloid staminodia is very characteristic, commonly
only one stamen being functional and even this one being peta-
loid. In nearly every case, also, there is a labellum, formed
either by the perianth or the staminodia. The habit of the vege-
tative body, however, is most peculiar. The real stem is a rhi-
zome, but the enormous leaves, differentiated into sheath, peti-
ole, and pinnately veined blade, build up a false stem by means
of their very large and closely overlapping sheaths.

The temptation is to derive this alliance from the Dracaena
region of the Liliaceae, but important anatomical features that
are common to all four families are opposed to this view. That
it is connected in some way with the Glumales-Farinales-Lil-
ales stock seems most probable; and if so the general structures

* SciTaMINEAE of Engler.

MORPHOLOGY OF ANGIOSPERMS

indicate a separate origin from Glumales. A morphological
investigation of these families in the tropics is greatly to be
desired.

X. Orcurpares.*—The two families of this alliance are
Burmanniaceae and Orchidaceae, all but about 55 of the 7,000
species belonging to the latter family. These two unequal fami-
lies are held together by the very numerous and small ovules
and by the extreme zygomorphism of the flower, but the Bur-
manniaceae have endosperm, often six stamens, and frequently
connate perianth-segments, ap] es the Amaryllidaceae.

The chief interest of the alliance centers about the Orchi-
daceae, the greatest monocotyledonous family im point of spe-
cies and the most highly specialized. The epiphytic habit is
extensively developed, and the terrestrial forms are iostly
saprophytic or parasitie. These habits have resulted in the
development of certain special structures, such as the lulbous
leaf-bases and velamen of the epiphytic forms; and in the sup-
pression of some normal structures, as the primary root, and
sometimes all roots. The absence of endosperm, the poorly
developed embryo, and the extensive use of the suspensor as a
remarkably developed haustorial organ are probably but addi-
tional results of the nnusual habits of the family. The notable
floral structures are the modification of one of the petals to
form the labellum and spur, the remarkable ‘t gynostemium,”
the twisted ovary, and the pollinium-mechanism.

As an illustration of the varying modifications of floral
structure, the ordinary orchid may be compared with the Cy-
pripedium type. The Howers are pentaeyelic, and the cycles
are developed im the two types as follows, beginning with the
outermost. In both types the first evcle consists of three sepals,
and the second of three petals, the posterior (made anterior by
the twisting of the ovary) forming the labelluam and spur. In
the third cycle two lateral stamens are sup pressed in both types,
but im ordinary orchids the anterior one is functional, while
in Cypripedium it is replaced by a staminodium. Tn the fourth
eycle the posterior staimen is suppressed in both types, but in
ordinary orchids the two laterals are replaced by staminodia,
while in Cypripedium they are functional stamens. Tn the

* MicrosperMan of Engler.

CLASSIFICATION OF MONOCOTYLEDONS 239

fifth cycle in ordinary orchids the two lateral carpels form the
stigma, the anterior producing the disk-bearing “ rostellum,”
while in Cypripedium all three carpels form the stigma.

The origin of the Orchidaceae is very obscure. It is com-
mon to regard them as derived from the Liliales, but there are
many objections to this hypothesis. In any event, it seems
most natural to refer them to the same general stock.

According to the views presented in this chapter, there are
three primitive monocotyledonous stocks—Pandanales, Helobi-
ales, and Glumales—and they are connected with the other
alliances as follows: Pandanales-Palmales-Synanthales; [Helo-
biales-Arales; Glumales-Farinales-Liliales-Scitaminales-Orchi-
dales.

CHAPTER XI

CLASSIFICATION OF ARCHICHLAMYDEAE

Two great divisions of Dicotyledons are evident, the Archi-
chlamydeae and Sympetalae, although there is no sharp distine-
tion between them. Sympetalous forms among the former and
polypetalous forms among the latter occur, but in the main
apetaly or polypetaly is a distinctive feature of the Archichla-
mydeae, and sympetaly of the Sympetalae. That the Archi-
chlamydeae include the most primitive Dicotyledons is clear,
but what forms are to be regarded as the most primitive is open
to discussion.

The classification of the Archichlamydeae is an exceedingly
puzzling problem, and the current schemes are far less detinite
and satisfactory than those for the classification of Monocotyle-
dons and Sympetalae. Questions of primitive and reduced
characters, and of relative rank on the basis of combination of
characters, are particularly involved among Archichlamydeae,
and henee opinions vary widely as to the details of their classi-
fication. The ditheulties arise from the fact that the characters
of the group are extremely fluctuating, not being established
as among the Sympetalae. Add to this that more than 60,000
species *

are recognized, over three times as numerous as the
species of Monocotyledons, ineluded in 180 families, and it
becomes evident that the confusion of relationships is bewil-
dering.

Eneler has arranged the Avehichlamydeae in twenty-six al-

*'The numbers of species given in this chapter must be regarded as approx-
imate and conservative. They will vary with the increase of knowledge and
the conception of species, but in this chapter they are only intended to indi-
cate the relative display of different types of structure. ,

240

CLASSIFICATION OF ARCHICHLAMYDEAE 241

lances, coordinate with the ten series of Monocotyledons. The
general sequence of these alliances is based, as in Monocotyle-
dons, upon the development of the perianth and of the floral axis,
and the arrangement of floral members; but other characters,
chiefly those derived from the ovules, are also used to disen-
tangle relationships. Of course there is no real sequence ot
these twenty-six alhances, for they represent, for the most part,
parallel or divergent lines of development. The sequence of
presentation is determined in the main by the relative advance-
ment of the lower members of each alliance, whose higher meim-
bers may or may not have made great advancement and in many
directions. Such an assemblage of forms may be conceived of as
a tangled thicket, through which certain paths may be more or
less evident, but in which no orderly arrangement is apparent.
It would be confusing, even were it possible, to discuss the
relationships of each of the twenty-six series. They can only
be presented as assemblages of families that seem to be natural,
perhaps not so much on account of their common origin as on
account of their approximately equal grade of advancement,
and hence “ form-groups” rather than necessarily genetic
groups.

The folowing presentation of the alliances of Archichlamy-
deae is largely based upon Engler’s “* Uebersicht iiber die Unter-
abteilungen, Klassen, Reihen, Unterreihen, und Familien der
Embryophyta siphonogama,” published in Engler and Prantl’s
Die Natiirlichen Pflanzenfamilien in 1897 (Lieferung 165).

The first twelve alliances are especially puzzling. Among
them are evidently the most primitive forms in floral structure.
They also include the chalazogamic forms, and ovules whose
structure is unusual among Angiosperms. The families are
practically those that were disposed of by Eichler as Amen-
tiferae, together with miscellancous groups of uncertain afhnity.
That the so-called Amentiferae or Amentaceae represented a
heterogeneous assemblage of forms has long been evident. It is
a question whether Engler’s splitting up into alliances has not
been excessive in this part of his scheme, certain morphological
characters sometimes being used that may not prove to be of
first importance. In any event, the sphtting up will serve to
keep apart distinet groups until they can be recombined natu-
rally. There is no region of the Archichlamydeae which has

242, MORPHOLOGY OF ANGIOSPERMS

recently received more deserved attention from morphologists,
and whieh still so greatly needs investigation.

I. CasvarrvaLes.*—This includes the single family Casu-
arinaceae, containing about 25 species. Engler regards the al-
liance as the most primitive because the ovule develops miuner-
ous inegaspores. This particular character can not be regarded
as distinetive, since among the Fagales the same character,
associated also with chalazogamy, occurs, and numerous mega-
spores are found among the Ranales, Rosales, ete. The low
position, however, is justified by the primitive flowers, which
are either naked or with a bract-like perianth.

The next two alliances are regarded as relatively primitive
on account of their naked flowers, together with the Casnari-
nales being the only naked alliances.

Il. Preerares.—This includes the Saururaceae, Pipera-
ceae, Chloranthaceae, and Lacistemaceae, together containeg
about 1,150 species, of which about 1,100 belong to the Pipera-
ceae. The results of the investigation of Peperomia pellucida
by Campbell and by Johnson indicate that the tropical Pipera-
eeae are probably most promising forms for morphological
investigation, and are to be considered in any diseussion as to
the most primitive Dicotyledons.

III. Sarrcares.—This includes the single family Salica-
ceae, containing about 180 species.

TV. Myricares.—This includes the single family Myrica-
cere, containing +0 species. The adyanee in floral structure is
shown by the fact that the several bracts near the flower may
be regarded as an extremely primitive perianth.

V. Baranorvsrpates.—This ineludes the single family Ba-
lanopsidaceae, containing 7 species. This is an uncertain type,
and raises the question of reduction. The staminate flowers
have a rudimentary perianth and an indefinite number of sta-
mens; and the earpellate flowers have a bracteate perianth.
Engler calls attention, however, to the fact that there are no
intermediate forms for a reduction series, and that the indefi-
nite number of stamens is a primitive character.

VI. Lerryerrares.—This ineludes the single family Leit-

neriaceae, contaiming 2 species. The primitive character of this

* VeRTICILLATAE of Engler.

CLASSIFICATION OF ARCHICHLAMYDEAE 243

type, with its flowers naked or with a bracteate perianth, is
very doubtful. Engler states that if any evidence of reduction
is obtained, this family would be included among the Rosales,
near the Hamamelidaceae.

VIL. JuGraypares.—This includes the single family Ju-
glandaceae, containing about 30 species. This alliance is dis-
tinctly higher than the preceding ones in that there is nearly
always a distinet perianth, which in the carpellate flowers is
coalescent with the ovary, so that there is a resemblance to
epigyny. Disregarding the Balanopsidales and Leitneriales as
doubtful and possibly reduction alliances, the Juglandales are to
be compared directly with the Myricales. The two were for-
merly associated in a single alliance, but the distinct perianth,
as well as chalazogamy, serve to distinguish the Juglandales.
It is a question whether such differences, and the others asso-
ciated with them, are incompatible in a single alliance.

VIII. Facares.—This includes the Betulaceae and Faga-
ceae, together containing about 420 species, nearly 350 of which
belong to the Fagaceae. This is a parallel alliance with Juglan-
dales, having a distinct but bracteate perianth, which in the
carpellate flowers is more or less coalescent with the ovary.
Among Betulaceae, also, chalazogamy occurs, as in Juglanda-
ceae and Casuarinaceae.

LX. Urrreanes.—This includes the Ulmaceae, Moraceae,
and Urticaceae, together containing about 1,560 species, the
large families being Moraceae with about 920 species, and the
Urticaceae with about 520. This is an alliance parallel with
the Juglandales and Fagales, with the distinct and bracteate
perianth, which, as in Fagales, is definitely cyclic.

X. Proreates.—This includes the single great Australasian
family Proteaceae, with about 950 species. In this ailiance
the next stage in the development of the cyclic perianth becomes
evident. Although it is sometimes green and bract-like, in the
majority of cases it is petaloid, but there is no differentiation of
calyx and corolla. A character used to distinguish this alliance
from the following is the single carpel with well-developed
ovule.

XI. Sawrararnes.—This includes the Loranthaceae, Myzo-
dendraceae, Santalaceae, Grubbiaceae, Opiliaceae, Olacaceae,
and Balanophoraceae, together containing about 1,260 species,

O44 MORPHOLOGY OF ANGIOSPERMS

the large families being Loranthaceae with 800 species, Santa-
laceae with 246, and Olacaceae with 150. In this alliance, also,
the eyelie perianth is for the most part petaloid, but there is
advancement in the general differentiation of a calyx and co-
rolla. For the most part, there is a synearpous pistil of three
carpels, but the carpels may be two or one; and a free central
placenta develops ovules without an integument or no distinct
ovules at all. There is much diversity within the alliance, at
least three distinct lines being evident; but the rather remark-
able morphological structures found in the alliance are prob-
ably related to their general parasitic or semi-parasitic habits.

ATI. Artsrorocitares.—This includes the Aristolochia-
ceae, RatHesiaceae, and ILydnoraceae, together containing about
2535 species, of which 205 belong to the Aristolochiaceae. The
members of this series are distinctly in advance of the preceding
in the coalescence of the petaloid segments of the perianth, and
especially in epigyny. The indefinite number of ovules is also
a distinguishing feature.

The preceding twelve alliances represent a primitive com-
plex, im which reduced forms may have been included. How
they may be related to one another in origin is too obscure for
profitable discussion, but it scems probable that they are not at
all related to the following allianees. In other words, whether
they represent a single genetic stock or several, they appear to
be isolated from the higher alliances.

XII. Poryeconarrs.—This ineludes the single family
Polygonaceae, with about 750 species. Its mostly eyelie
flowers, with undifferentiated perianth or distinct calyx and
corolla, puts it upon about the plane of advancement attained
hy the preceding alliances; while its strong trimerous tendency
and peculiar habit set it well apart. This is sometimes re-
garded as a transition group between the preceding alliances
and the Centrospermales. In any event, it may be regarded
as fairly associated with the latter.

ATV. CrenrrosperMates.* — This includes Chenopodia-
ceae, Aimarantaceae, Nvetaginaceae, Batidaceac, Cynoeramba-
ceae, Phytolaceaceae, Aizoaceae, Portulacacene, Basellaceae, and

9

Carvophyllaceae, together containing about 3,320 species, the

* CENTROSPERMAE of Engler,

CLASSIFICATION OF ARCHICHLAMYDEAE 245

large families being Caryophyllaceae with 1,420 species, Aizoa-
ceae with 575, and Chenopodiaceae and Amarantaceae each
with about 455. In this alliance the floral characters range
from the bracteate undifferentiated perianth of Chenopodiaceae
to the distinct calyx and corolla of many Caryophyllaceae. In
the alliance as a whole calyx and corolla are frequently rather
than prevailingly distinct, and only the highest family has at-
tained the conspicuous corolla associated with entomophily. A
feature ot the alhance is the conspicuous perisperm.

The Polygonales and Centrospermales may possibly have a
closely related origin, but it does not seem probable that they
are related in any way to the following alliance, but that they
represent a general line of development whose highest expres-
sion is among the Caryophyllaceae.

XV. Rayates.—This includes Nymphaeaceae, Ceratophyl-
laceae, Trochodendraceae, Ranunculaceae, Lardizabalaceae, Ber-
beridaceae, Menispermaceae, Magnoliaceae, Calycanthaceae, Lac-
toridaceae, Anonaceae, Mvristicaceae, Gomortegaceae, Monimia-
ceae, Lauraceae, and Hernandiaceae, together containing about
4,050 species, the large families being Lauraceae with 1,015
species, Ranunculaceae with 990, Menispermaceae with 390,
Anonaceae with 345, Monimiaceae with 245, Myristicaceae with
235, and Berberidaceae with 135.

This great alliance introduces the prevailing habit of a dis-
tinct calyx and corolla, and is characterized by the prevalence
of apocarpy and hypogyny. The primitive character of the
flower is indicated not only by apocarpy and hypogyny, but also
by the strong tendency to the indefinite repetition and spiral
arrangement of the floral members. Were it not for the preva-
lence of a distinet calyx and corolla the alliance would not hold
so high a rank. At least three prominent developmental lines
are evident, viz., Nymphaeaceae to Ceratophyllaceae, Ranun-
culaceae to Menispermaceae, and Magnoliaceae to Tlernandia-
ceae. In each of these lines there is an advance from the
spiral to the cyclic arrangement, and in the last line epigyny
is reached. As is also known, zygomorphy occasionally occurs,
being present in no preceding alliance except the Aristolochiales.

It seems probable that the higher alliances of the Archichla-
mydeae are related in some way to the Ranales, whose numerous
lines of development seem to have been taken up by other

246 MORPHOLOGY OF ANGIOSPERMS

allauces. It follows that the subsequent alliances will touch the
Ranules in various ways, the latter representing a plexus out of
which various divergent lines have become distinct. This con-
ception of the genetic position of Ranales among Archichlamy-
deac has brought to them the attention of morphologists, and
the results thus far have more than justified their investigation.

XVI. Rirozpares.—This includes Papaveraceae, Cruci-
ferae, Tovariaceae, Capparidaceae, Resedaceae, and Moringa-
ceae, together containing about 2,615 species, the large families
being Cruciferae with 1,860 species, Capparidaceae with 425,
and Papaveraceae with 280. There seems to be no question
that this alliance is closely related to the Ranales. The connec-
tion seems to be through the Papaveraceae, which exhibit struc-
tures resembling those of Nymphaeaceae; while the transition
from Papaveraceae to Cruciferae through the Mumaria forms
is plain, and the affinity of Cruciferae and Capparidaceae is
unquestioned.

XVII. Sarracentares. — This includes Sarraceniaceae,
Nepenthaceae, and Droseraceae, together containing 145 spe-
cies, nearly 100 of which belong to the Droseraceae. The
alliance is evidently parallel with Rhoedales, and both are cer-
tainly related to the Nymphaeaceae-region of the Ranales. In
fact, the Nymphaeaceae, Papaveraceae, and Sarraceniales have
many things in common in the arrangement of floral members
and the spiroeyclic character of the flowers. The distinctive
character of Sarraceniales as compared with Rhoedales is the
prevalence in the former of central placentation.

XVIII. Rosares.—This includes Podostemonaceae, Ily-
drostachyaceae, Crassulaceae, Cephalotaceae, Sanifragaceae,
Pittosporaceae, Brunelliaceac, Cunoniaceac, Myrothamnaceae,
Bruniaceac, Hamamelidaceac, Platanaceae, Crossosomataceae,
Rosaceae, Connaraceae, and Leguminosae, together containing
about 14,270 species, the large families being Leguminosae with
over 11,000 species, Rosaceae with 1,525, Saxifragaceae with
630, and Crassulaceae with 490. Since this allianee contains
by far the greatest family of Archichlamydeae, in fact, with a
single exception, the greatest family of Angiosperms, it may
be regarded as the most representative and dominant alliance.

The beginnings of this great alliance, with apoearpy, hypo-
gyny, and indefinite repetition of certain floral members, have

CLASSIFICATION OF ARCHICHLAMYDEAE 247

much in common with the Ranales, especially the line con-
taining Ranunculaceae. However, it has reached a much higher
development in the more frequent occurrence of syncarpy, and
also of perigyny and epigyny, and especially in the remarkable
development of zygomorphy among the Leguminosae. Disre-
garding the smaller families, the Saxifragaceae may be regard-
ed as the beginnings of the alliance, originating in the Ranales,
and diverging toward Podostemonaceae in one direction and
Rosaceae-Leguminosae in the other. It has long been known
that there is no real distinctive character separating Saxifraga-
ceae and Rosaceae; and the transition from the latter family to
the Leguiminosae is easy. Rosaceae are characterized by actino-
morphic flowers and several carpels; while Leguminosae have
zygomorphic flowers and a single carpel; but there are members
of the two families that exactly reverse these distinctions. There
seems to be a general plexus formed by the Rosa tribe of Rosa-
ceae and the J/imosa tribe of Leguminosae, which is not very
far removed from the Ranunculaceae among Ranales. Out of
the Rosa tribe the two very distinct lines of drupe-forms and
pome-forms have diverged; while the A/imosa tribe, with its
actinomorphic flowers and numerous usually free stamens, leads
through the Caesalpinia tribe, with its actinomorphie or zygo-
morphie flowers and free stamens, to the Papilio tribe with its
strongly zygomorphiec flowers and coalescent stamens.

The culmination of the alliance is of course the elaboration
of zygomorphy, the Leguminosae dominating in this regard
among Archichlamydeae, as do the Orchidaceae among Monoco-
tyledons, and the Personales among Sympetalae.

In the preceding related alliances, from Ranales to Rosales,
the cyclic character of the flower is not fully established, every
line of development having spiral members. In the following
alliances, however, the cyclic character is fully established.

XIX. Gerantates.—This includes Geraniaceae, Oxalida-
ceae, Tropaeolaceae, Linaceae, IJumiriaceae, Erythroxylaceae,
Zygophyllaceae, Cneoraceae, Rutaceae, Simaruhaceae, Bursera-
ceae, Meliaceae, Malpighiaceae, Trigoniaceae, Vochysiaceae,
Tremandraceae, Polygalaceae, Dichapetalaceae, Euphorbiaceae,
and Callitrichaceae, together containing about 9,160 species,
the large families being Euphorbiaceae with 4,140 species, Ru-
taceae with 910, Meliaceae with 753, Malpighiaceae with 700,

als

248 MORPHOLOGY OF ANGIOSPERMS

Polygalaceae with 667, Geraniaceae with 455, Oxalidaceae with
350, and Burseraceae with 320,

This cyclic alliance begins with those families that are iso-
carpic and extends to those in which a reduction in the number
of carpels is prevalent. It is chiefly distinguished from the
Sapindales, with which it is parallel and very closely alhed,
by the orientation of the ovules, the raphe of the anatropous
ovules being ventral in Geraniales and dorsal in Sapindales.
Just the significance of such a character in distinguishing great
genetie alliances is not clear, but its constancy is in its favor,
Three lines of development are evident, the most prominent
beginning with Geraniaceae, including the zygomorphic and
anisocarpic Tropaeolaceae and the completely synearpic Lina-
ceae and its allies, and ending in Cneoraceae to Mehaceae with
oil-cells and highly differentiated tissues. Another line is Mal-
pighiaceae to Vochysiaceae, characterized by oblique zygomor-
phy; while Polygalaceae with its strongly zygomorphic flowers,
Dichapetalaceae, and Euphorbiaceae, show no surviving fea-
tures in common. The affinities of these last three families
are extremely doubtful, and those of Callitrichaceae are even
more so.

XX. Sapmypares.*—This includes Buxaceae, Empetra-
ceae, Coriariaceae, Limnanthaceae, Anacardiaceae, Cyrillaceae,
Pentaphylaceae, Corynocarpaceae, Aquifoliaceae, Celastraceae,
Hippocrateaceae, Stackhousiaceae, Staphyleaceae, Leacinaceae,
Aceraceae, Hippocastanaceae, Sapimdaceae, Sabiaceae, Meh-
anthaceae, and Balsaminaceae, together comprising about 3,125
species, the large families being Sapindaceae with 1,040 species,
Celastraeceae with 425, Anaeardiaceae with 395, Balsaminaceae
with 300, and Aquifoliaceae with 285.

As among Geraniales, the alliance begins with isocarpic
forms and passes to those in which the number of carpels is
reduced, and in the higher families zygomorphy is attained.
The orientation of the ovules that separates this alliance from
the Geraniales was referred to under that alliance. Engler ree-
ognizes so many lines of development among Sapindales that
the alliance seems to be well broken up, and the different mem-
bers not elearly related to one another.

* Sometimes called CELASTRALES.

CLASSIFICATION OF ARCHICHLAMYDEAE 249

XXII. Ruamnares.—This includes Rhamnaceae and Vita-
ceae, together containing about 955 species, almost exactly
equally distributed between the two families. The alliance is
clearly parallel with the preceding one, but is distinctly set
apart by its tetracyclic flowers with opposite stamens.

XXII. Marvares.—This includes Elaeocarpaceae, Chlae-
naceae, Gonystylaceae, Tiliaceae, Malvaceae, Triplochitonaceae,
Bombacaceae, Sterculiaceae, and Scytopetalaceae, together con-
taining about 1,740 species, the large families being Malvaceae
with about $00 species, and Stereuliaceae with 780. This
alliance is very uneven in the advancement of its characters, and
in certain features would seem to precede Geraniales and Sa-
pindales in any sequence; but it is so closely related to Parie-
tales through Elaeocarpaceae and Chlaenaceae that it seems
clear it should be placed near them.

Distinct or slightly united carpels are found, as among the
Geraniales and Sapindales, but complete synearpy prevails.
The inequality of advancement is shown in such families as
Tiliaceae, in which there is complete synearpy associated with
indefinite stamens; and Sterculiaceae, in which there is a com-
plexity in the arrangement of stamens approaching that in
Malvaceae, associated with a more or less incomplete union of
carpels.

XXIII. Parretrares.—This ineludes Dilleniaceae, Eu-
cryphiaceae, Ochnaceae, Caryocaraceae, Maregraviaceae, Qui-
inaceae, Theaceae, Guttiferae, Dipterocarpaceae, Elatinaceae,
Frankeniaceae, Tamaricaceae, Fouquieraceae, Cistaceae, Bixa-
ceae, Cochlospermaceae, [oeberliniaceae, Canellaceae, Viola-
ceae, Flacourtiaceae, Stachyuraceae, Turneraceae, Malesherbia-
ceae, Passifloraceae, Achariaceae, Caricaceae, Loasaceae, Datis-
caceae, Begoniaceae, and Ancistrocladaceae, together compris-
ing about 4,225 species, the large families being Guttiferae
with 760 species, Flacourtiaceae with 525, Begoniaceae with
405, Violaceae with 400, Dipterocarpaceae with 320, and Pas-
sifloraceae with 315.

The Parietales are prevailingly synearpous, and have very
evident connection with the Ranales through the Dilleniaceae,
which were formerly included among the Ranales, and with
the Rhoedales through the Flacourtiaceae and other families.
The families from Dilleniaceae to Dipterocarpaceae, mainly

250 MORPHOLOGY OF ANGIOSPERMS

tropical, are regarded as one line, characterized by an oily en-
dosperm; and among them such primitive characters as the
spiral arrangement and indefinite number of floral members
occur, and even apocarpy (Ochnaceae). Another line includes
the Elatinaceae to the Frankeniaceae, chiefly a temperate group
characterized by a starchy endosperm. The Fouquieraceae are
regarded as independent of the last lne on account of their
sympetaly and oily endosperm. The Cistaceae and Bixaceae
also form an independent line with starchy endosperm. The
Cochlospermaceae and IXoeberliniaceae are also regarded as
independent and much resemble the Capparidaceae among: the
Rhoedales. The families from Canellaceae to Achariaceae form
another line, all characterized by oily endosperm, starting with
completely cyclic flowers, and leading to such special develop-
ments as a strong tubular development of the receptacle and
even sympetaly (Achariaceae). Closely related to this line are
the Caricaceae, with sympetalous corollas, but distinguished by
their stamens and latex system. The last four families (Loasa-
ceae to Ancistrocladaceae) are epigynous, but each one seems to
be a peculiar and isolated type of development. This complex
alliance is a good illustration of divergent lines of development
within one general circle of affinity, and at the same time of a
gradual increase in floral complexity.

XAIV. Opuntiares.—This includes the single family
Cactaceae, with about 1,000 species. This characteristic Amer-
ican family presents a strange mixture of primitive and ad-
vanced characters in the structure of the flower. The spiral
arrangement and indefinite repetition of floral members are
often as primitive as in the Nymphaeaceae, with which region
of the Ranales the alliance may be connected. The tubular
receptacle, however, enclosing the constantly synearpous pistil
relates the group to the Parietales.

XAV. Myrrares.—This includes the Geissolomaceae, Pe-
hacaceae, Oliniaceae, Thyimelaeacene, Elacagnaceae, Lythra-
coae, Souneratiaceac (Blattiaceae), Punieaceae, Leeythidaceae,
Rhizophoraceae, Combretaceac, Myrtaceae,’ Melastomataceae,
Onagraceae, Wydrocaryaceae, Haloraghidaceae, and Cynomo-
riaceae, together containing about 7,180 species, the laree fami-
hes being Melastomataceae with 2,750 species, Myrtaceae with
2,965, Onagraceae with 465, Thymelaeaceae with 395, and

CLASSIFICATION OF ARCHICHLAMYDEAE 251

Lythraceae with 340. The high character of this alliance is in-
dicated by the constantly perigynous and epigynous flowers, as
well as by the constantly cyclic stamens, and the tendency to
tetramerous flowers is strong.

XXVI. Umperrares.*—This includes the Araliaceae,
Umbelliferae, and Cornaceae, together containing about 2,660
species, about 2,100 of which belong to the Umbelliferae. The
series is clearly the ranking one among the Archichlamydeae on
account of its epigyny, cyclic stamens, reduced number of car-
pels, and mostly reduced sepals, the floral formula being the
same as that of the highest Sympetalae. The three families
constituting the alliance are very closely related, and the alliance
as a whole stands so stittly apart from other Archichlamydeae
as to raise the question whether it does not really belong among
the higher Sympetalae.

It will be noted that in a large sense, and with the excep-
tion of the last two alliances, the Archichlamydeae correspond
to the Spiral series among Monocotyledons, in which the cycle
arrangement, although it frequently appears, is not fully estab-
lished in every set of floral members. In the same sense, there-
fore, the Myrtales, Umbellales, and Sympetalae, correspond to
the Cyclic series among Monocotyledons.

* UMBELLIFLORAE of Engler.

CHAPTER XII
CLASSIFICATION OF SYMPETALAE

Tue Sympetalae form a much better defined group than do
the Archichlamydeae, from which they seem to have been de-
rived. The sympetalous character is almost universal, and
justifies the name of the group. To regard it as the crucial
test, however, is to introduce the flavor of an artificial system.
Among the Archichlamydeae sympetalous forms were noted,
and certain familes of the Sympetalae include polypetalous
members. It would seem that such exceptions might apply to
whole families, whose other characters would determine their
attinities. For example, the Umbelliferae present the combina-
tion of characters that belongs to the Sympetalae, excepting
svinpetaly; and this exception does not seem to be a suthcient
reason to exclude them from association among the epigynous
anisocarpic Sympetalae, any more than the polypetaly of the
Pirolaceae excludes them from the isocarpie Sympctalae.

The general characters of Sympetalae are (1) a complete
eyche arrangement of the floral members, associated with defi-
nite numbers; (2) a sympetalous corolla that usually has a
common origin with the stamens; and (3) ovules with a single
massive integument and a very small nucellus. The group con-
tains fifty-one families, the number varying with different av-
thors, and about 42,000 species, or approximately two-thirds
of the number included in the Nrehichlamydeae. Eight alli-
ances have heen recognized by Engler, coordinate with the ten
alliances of Monocotyledons and the twenty-six alliances of
Archichlamydeae, the contrast with the latter group in wniform-
ity of floral structure being very striking.

The natural sequence of the alliances is much more evident
than among the Archichlamydeae. The first three alliances are

CLASSIFICATION OF SYMPETALAE 253

pentacyclic and isocarpic, while the remaining five are tetra-
cyclic and anisocarpic; and of the anisocarpic alliances, the first
three are hypogynous and the last two epigynous.

The three pentacyclic or isocarpic alliances are certainly
most nearly allied to the Archichlamydeae, for among them poly-
petaly still occurs, the two cycles of stamens are characteristic,
and occasionally the ovule has two integuments. They may be
regarded as lines from the Archichlamydeae in which sympetaly
has become prevalent. They are all hypogynous and actino-
morphic, and the floral formula is characteristically sepals 5,
petals 5, stamens 5 + 5, carpels 5. These comparatively primi-
tive Syimpetalae are not numerous, containing only about 3,500
of the 42,000 species, and hence they are not the representative
Sympetalae.

J. Ertcares.—This includes the Clethraceae, Pirolaceae,
Lennoaceae, Ericaceae, Epacridaceae, and Diapensiaceae, to-
gether containing a little more than 1,700 species, by far the
largest family being Ericaceae with about 1,360 species. The
group is characteristically developed in high latitudes and alti-
tudes, and its special features are well marked. The stamens
are usually quite free from the petals, and this in connection
with occasional polypetaly gives a strong resemblance to the
Archichlamydeae; while the peculiar dehiscence of the anthers
and their frequent appendages are very characteristic. The
stamens are by no means constantly in two cycles, or distinct
from the corolla or one another. <A single cycle of functional
stamens may be associated with staminodia, or only a single
cycle may appear, or the stamen cycle may have a common ori-
gin with the corolla, or in some cases it may be monadelphous.
In short, there are transition forms to the suppression of a cycle
of stamens, and to a common origin of stamen cycle and corolla.
A multilocular ovary with numerous ovules is also a feature of
the alliance.

The Epacridaceae, a well-developed Australian family of
heath-like plants containing nearly 300 species, are quite ex-
ceptional in having only one cycle of stamens and anthers with
longitudinal dehiscence. These exceptions seem quite funda-
mental, but they may be illustrations of the result of long and
distant separation of allied families. In any event, a com-
parative morphological study of Epacridaceae and Ericaceae

254 MORPHOLOGY OF ANGIOSPERMS

is much needed; and the whole series of Ericales deserves atten-
tion on account of its possible genetic connections with some
region of the Archichlamydeae.

IL. Priwurares.—This includes the Myrsinaceae, Primula-
ceae, and Plumbaginaceae, together containing about $50 spe-
cies, approximately equally distributed among the three faimi-
lies. The families are closely associated in structure, but
widely separated in geographical distribution, the Myrsinaceae
being characteristically tropical trees and shrubs (chietly Amer-
ican), the Primulaceae north temperate and boreal herbs, and
the Phunbaginaceae characteristically halophytic herbs and un-
dershrubs of salt-beaches and steppes (chietly Mediterranean
and Caspian). That such dissociated familes should have so
much in common is a strong argument against the older idea
that similarity of structure proves common origin.

The two most characteristic features of the group are the
single cycle of stamens opposite the petals, and the unilocular
ovary with its “ free central placenta ” bearing numerous ovules.
The single cycle of stamens and its opposition to the petals are
explained by the frequent occurrence of rudiments representing
an outer abortive cycle. The “ free central placenta” of tax-
onomists 18 of course a continuation of the floral axis to bear
ovules, and is perhaps the most important morphological char-
acter of the series. It is in this group, also, that there has been
noted a peculiar origin of the petals, which are said to arise
late from the primordia that have already developed the
stamens.

As compared with the Erieales, the Primulales may be re-
garded as somewhat more advanced toward the higher Syvmpeta-
lae, but polypetaly still oceurs among them, and they give the
impression of a somewhat divergent and specialized eroup. An
investigation of the Myrsinaceae will doubtless result in a much
clearer understanding of the relationships.

Ill. Esenates.—This includes the Sapotaceae, Ebenaceae,
Styracaceae, and Symplocaceae, together containing nearly 900
species, the large families heing Sapotaceae with about 380 spe-
cies, and Ebenaceae with 275. The group is chiefly developed
in the tropies and the species are all shrubs or trees.

The alliance is partienlarly puzzling in its affinities, since
there is a combination of primitive and advanced characters.

CLASSIFICATION OF SYMPETALAE 255

The primitive characters are the indetiniteness in the number
of sepals and petals, ranging from 4 to 8, occasional polypetaly,
and the often numerous stamens and carpels. Consistency
would seem to demand that the Ebenales be regarded as the
most primitive of the Sympetalae, even the definite cyclic num-
bers not being established. At the same time, there is adherence
of a single stamen cycle to a sympetalous corolla, and distinct
epigyny. The stamen cycles are peculiarly fluctuating, ranging
from three or four cycles, through all stages of suppression of
the outer cycles, to a single opposed cycle. ‘This latter feature is
suggestive of the Primulales, but the multilocular ovary with
usually large solitary ovules is suggestive neither of Primulales
nor Ericales. The tropical forms certainly deserve careful mor-
phological investigation, and are doubtless related to the Myr-
sinaceae, and in our judgment are to be included in any discus-
sion of the most primitive Sympetalae.

In the five following alliances the tetracyclic character seems
to be well established, and the prevailing formula is sepals
petals 5, stamens 5, carpels 2. In the three previous isocarpie
mllpaniees there is every transition from the pentaeyelic to the
tetracyclie condition, and among the more primitive anisocarpic
families the carpels are often three before two becomes the
established number. Of the remaining alliances the first three
are hypogynous.

IV. Gentranares.*—This includes the Oleaceae, Salyado-
raceae, Loganiaceae, Gentianaceae, Apocynaceae, and Asclepia-
daceae, together containing about 4,200 species, the large fami-
lies being Asclepiadaceae with about 1,720 species, Apocyna-
ceae ors 975, and Gentianaceae with 725.

With this alliance the grouping into developmental lines
becomes indefinite and perplexing, for the numerous families
intergrade in every direction. There is no distinctive character
that separates this alliance from the great alliance Tubiflorales.
The fact that the corolla is generally twisted in aestivation
seems to be the most useful character, and has suggested a name
for the series, and the constantly opposite leaves is a supple-
mentary character.

The lower members of the alliance are the Oleaceae and

* ConTorTak of Engler.

256 MORPHOLOGY OF ANGIOSPERMS

Salvadoraceae, in which there is sometimes distinct polypetaly,
but the reduction of the stamens to two in the former family
is hardly to be regarded as a primitive character. The Logania-
ceae are general in their resemblances, having features im com-
mon with the remaining families, and others suggestive of Tu-
biflorales and Rubiales. In fact, Engler suggests that the
Loganiaceae may be an older type than any of the others, and

may have given rise to the Gentianales and Rubiales, in which
he might have included the Tubiflorales. If this family may
hold any such position in reference to these great alliances it
certainly deserves careful investigation. The alliance ends with
the Apoevnaceae and Asclepiadaceae, in which a latex-system
is developed, and other evidences of high specialization occur ;
but they are also characterized by distinct carpels, a feature re-
garded as primitive. The Asclepiadiaceae form a very peculiar
and highly specialized offshoot, the elaboration of floral struc-
tures tor entomophily reaching a degree of complexity only to
be compared with that of the Orehidaceae.

V. Tuprrtorares.»—This includes Convolvulaceae, Pole-
moniaceac, Hydrophyllaceae, Borraginaceae, Verbenaceae, La-
biatae, Nolanaceae, Solanaceae, Serophulariaceae, Bignoniaceae,
Pedaliaceae, Martyniaceae, Orobanchaceae, Gesneraceae, Colu-
melliaceae, Lentibulariaceae, Globulariaceae, Acanthaceae,
Myoporaceae, and Phrymaceae, together containing over 14,600
species, the large families being Labiatae with nearly 3,000
species, Scrophulariaceae with 2,400, Acanthaceae with nearly
2,000, Solanaceae with about 1,700, and Borraginaceae with
about 1,550.

This enormous assemblage of forms has been ordinarily con-
sidered as representing at least two alliances, the Polemoniales
or Tubiflorae including the first four families of the list above,
and the Personales or Labiatiflorae including the remaining
families. The tendencies of development are so numerous and
interwoven that they are difficult to separate, but rather than
merge two such alliances together it might have been better to
have broken up the Personales into five or six alliances, espe-
cially it the Plantaginaceae are to be set off as a coordinate

alliance Plantaginales. To distinguish them definitely would

* TuBrrLoRAk of Engler.

CLASSIFICATION OF SYMPETALAE 257

probably be impossible, but an alliance at best expresses only a
general evolutionary tendency more or less completely worked
out.

Taking the alliance as a whole, it represents the culmination
of hypogynous Sympetalae, and this culmination is shown not
only in the conspicuous corolla but in highly developed zygo-
morphism. In tact, the Personales, with the Labiatae and
Scrophulariaceae as centers of aggregation, represent the great
zygomorphic group of the Sympetalae, as Leguminosae do
ainong the Archichlamydeae, and Orchidaceae among the Mono-
cotyledons.

First in the alliance are the Convolyulaceae and Polemonia-
ceae on account of their actinomorphic flowers and several-
ovuled carpels, in these and other features being, together with
the Gentianales, the least modified of the tetracyclic families.
From Gentianales they are easily distinguished by their lack
of twisted aestivation and by their usually alternate leaves, and
also by their undoubted relation to the other families of Tu-
bitlorales.

A second natural alliance is that formed by the Hydrophyl-
laceae and Borraginaceae, which leads from the preceding alli-
ance through Hydrophyilaceae, with a generally unlobed ovary,
to the Borraginaceae with a much modified ovary. In the latter
family the two carpels are divided by a false partition, each
loculus contains a single ovule, and the ovary becomes so deeply
lobed as to resemble a group of four nutlets. Further modi-
fications of this peculiar fruit, familiar to taxonomists, make
it the most specialized and diversified structure of this large
family.

A third natural alliance is that formed by the Verbenaceae
and Labiatae, with about 3,700 species. It is joined to the
Convolvulaceae by the orientation of the ovule, and has fol-
lowed a developmental path parallel with that of the preceding
alliance in the evolution of the carpel structures. The lobing
of the ovary into four nutlet-like bodies in the Labiatae, how-
ever, is not accompanied by such detailed specialization as in
the Borraginaceae; but the whole line is dominated by the
strong development of zygomorphy, reaching its culmination in
certain groups of the Labiatae.

A fourth natural alliance, the greatest of all, includes the

258 MORPHOLOGY OF ANGIOSPERMS

eleven families from Nolanaceae to Globulariaceae, grouping
about the Solanaceae and Scrophulariaceae. This series con-
neets with the Convolvulus forms through the Nolanaceae, but
does not develop its carpel-structures as do the Borrage and
Labiate lines, retaining capsules with numerous ovules, but
there is a strong development of zygomorphy.

To summarize at this point, the primitive stock of the series
seems to be the Convolvulaceae-Polemoniaceae alliance, from
which three distinct nes of development have diverged: the
Hydrophylaceae-Borraginaceae line, with its modified carpel-
structures; the Verbenaceae-Labiatae line, with its modified
carpel-structures and zygomorphy; and the Nolanaceae-Globu-
lariaceae line, with its zygomorphy. It should be noted in pass-
ing that the zygomorphy is associated with a strong tendency
to reduce the number of stamens.

The three remaining families are so peculiar in certain fea-
tures that Engler regards them as representing separate lines of
development, although the Acanthaceae are not easily separated
from certain families of the last alliance. The Myoporaceae
seem to be a reduced type with no clear athnities; and the
Phrymaceae, with their achenes and orthotropous ovules, have
no evident connections in this alliance, in which their strong
zygomorphy has retained them.

It would be our judgment, therefore, to break up this great
alliance of Tubiflorales into at least four, which might be ealled
the Polemoniales (Convolvulaceae and Polemoniaceae), Bor-
raginales (ILydrophyllaceae and Borraginaceae), Labiatales
(Verbenaceae and Labiatae), and Personales (Nolanaceae,
Solanaceae, Serophulariaceae, Bignoniaceae, Aecanthaceae, Pe-
daliaceae, Martyniaceae, Orobanchaceae, Gesneriaceac, Colu-
melliaceae, Lentibulariaceae, and Globulariaceae), the Myo-
poraceae and Phrymaceae being left undetermined or regarded
as reduction forms of Personales,

VI. Pranracryates.—This includes the single family
Plantaginaceae with about 200 species. This family, with its
pecuhar habit, 4-merous flowers, membranous corolla, and char-
acteristic fruit, is certainly entitled to special consideration.
Tf such a series as Tubiflorales be maintained, however, there
is no good reason why Plantaginaceae should not form one of
the seven or eight sections of it. If, on the other hand, the

; CLASSIFICATION OF SYMPETALAE 259

series be broken up as suggested above, Plantaginales should
certainly be coordinate with Polemoniales, Borraginales, Labi-
atales, and Personales.

The two remaining alliances are epigynous and naturally
form the culmination of the Sympetalae. In both alliances there
is actinomorphy and numerous ovules, but in both there is more
or less development of zygomorphy; a tendency to reduction
in numbers of members, especially of the ovules; and a tend-
ency to reduce the flowers in size and to mass them, leading
to a modification of floral structures and a differentiation of
the functions of individual flowers.

VII. Rusirates.—This ineludes the Rubiaceae, Caprifolia-
ceae, Adoxaceae, Valerianaceae, and Dipsaceae, together con-
taining nearly 4,800 species, the large family being Rubiaceae
with nearly 4,100 species.

The possible relationship of this alliance to the Gentianales,
especially the Loganiaceae, has been mentioned, from which
it seems to be an epigynous offshoot. At the same time, rela-
tions to the epigynous Umbellales among the Archichlamydeae
are no less evident. It may possibly be found, as intimated in
the last chapter, that the Umbellales should be associated with
the Rubiales as two parallel alliances of epigynous Sympetalae.
Through the Caprifoliaceae the Valerianaceae and Dipsaceae
are closely connected with the alliance ; while the position of the
Adoxaceae is altogether uncertain. The distinguishing char-
acter to separate Rubiales from the next alliance is not always
clear, but in general the connivent and often united anthers of
the Campanales are not present in the Rubiales; but this char-
acter is fortified by distinct developmental tendencies.

VIII. Caarpanares.—This includes the Cucurbitaceae,
Campanulaceae, Goodeniaceae, Candolleaceae, Calyceraceae,
and Compositae, together containing more than 14,500 species,
fully 12,500 of which are Compositae, the Campanulaceae con-
taining nearly 1,100.

Connivent and often united anthers, and sometimes mona-
delphous stamens, prevail in the series. The peculiar tropical
Cucurbitaceae occupy a special place in the alliance, and can not
be related clearly to the others; while the Campanulaceae seem
to represent a remnant of the ancient stock of the alliance, from
which the other families have arisen.

260 MORPHOLOGY OF ANGIOSPERMS

The alliance culminates in the Compositae, the greatest of all
angiospermous families, not only in rank, but also in the num-
ber of species, although not much exceeding the Leguminosae
in this latter regard. There seems to be no question that the
Compositae represent the highest expression of the various de-
velopmental lines we have been tracing through the Angio-
sperms. This is shown not merely in their combination of
sympetaly, epigyny, and seed-like fruit, but also by such special
structures as the pappus and the syngenesious anthers, by the
complex organization of the head, the prevalence of diclinism,

the dimorphism of corollas, ete.

CHAPTER XIII

GEOGRAPHIC DISTRIBUTION OF ANGIOSPERMS

So vast a subject can be presented only in very brief outline
in a single chapter. In a certain sense it is not pertinent to
a discussion of the special morphology of a group, but the stu-
dent of special morphology is aided by certain general consid-
erations connected with geographic distribution, especially in
any discussion of phylogeny. The distribution of a group con-
taining nearly 125,000 species includes a vast mass of details,
and only certain salient features can be selected for presenta-
tion. Even when these are selected, the numerous exceptions
to any general statement must be disregarded. It must be un-
derstood, therefore, that in the following account the statements
are very general in their nature, expressing average conditions
of distribution, under all of which exceptions may be cited.
At the same time, it is the general tendency in the distribution
of any large group that is of interest to the morphologist rather
than the details of distribution of species and genera.

The subject of geographic distribution presents two aspects
for consideration. One involves the determination of life-zones
over the surface of the earth, which is a eonsideration of dis-
tribution from the standpoint of physiography. The other
aspect disregards the life-zones, and considers distribution from
the standpoint of plant-groups. What a given plant-group has
heen able to do in the occupation of the earth’s surface is of
more morphological interest than the physiographic features
of the problem, and hence the following presentation will take
the latter standpoint.

Including only the existing vegetation gives a very inade-
quate conception of the relation of any group to the earth’s
surface. The present distribution of a group is only the last

261

262 MORPHOLOGY OF ANGIOSPERMS

stage in a long history of distribution, and a knowledge of this
history is an essential factor in any explanation of the present
distribution. Unfortunately, very little of this history is avail-
able, and this presentation must content itself with indicating
the present relation of groups to the earth’s surface, without
any attempt at explanation. This is particularly unfortunate,
since a lack of historical evidence may vitiate many conclu-
sions. If this lack of historical testimony be added to the
lack of any adequate record of the geographic distribution of
existing species, it becomes evident that the generalizations pro-
posed inust be of the most tentative character. With this ex-
planation the following statements may be given their proper
weight.

MONOCOTYLEDONS

Tt is possible to present the distribution of the ten alliances
of Engler in the order of their supposed relationship, a method
that may be of service in the subsequent consideration of the
ancient history and phylogeny of the group. One genetic group
is supposed to include the three following alliances.

Panpanates.—The Pandanaceae (screw-pines), apparently
the most primitive of Monocotyledons, belong to the general
region of the Indian Ocean. Associated with them in relation-
ship are the Typhaceae, found in aquatic conditions throughout
the world, but most abundant in the tropies; and the Spargania-
ceae, restricted to the temperate and boreal regions of the
northern hemisphere and also of the Australasian region, and
not represented in the tropics. The series as a whole shows
wide adaptations to temperature, but not to soil conditions, with
the primitive forms massed in the oriental tropics.

Parmaves.—The Palmaceae are about equally divided be-
tween the oriental and oecidental tropies, with no temperate
outliers, but not a species or a genus is common to the two
henuspheres. The geographical association of the palms and
screw-pines in the orient is in favor of their supposed relation-
ship, but the palms of the oeeident need explanation, especially
since Phylelephas, regarded as a genus intermediate between
Pandanaceae and Palmaceae, is an American genus. The pres-
ent distribution of palms is an excellent illastration of ie de-
velopment of continental diversities, which in this ease has

GEOGRAPHIC DISTRIBUTION OF ANGIOSPERMS 2638

resulted not only in distinct genera, but almost every tribe is
either oriental or occidental. Furthermore, the much larger
nuuber of monotypic genera in the orient must be associated
with its larger and more broken tropical area.

SynantuaLes.—The Cyclanthaceae are as restricted to
the American tropics as the Pandanaceae are to the oriental
tropics.

If this general “ palm” type, comprising these three alli-
ances, Was once connected in the two hemispheres by a northern
distribution, the palms alone found both hemispheres congenial
in the tropics, while the Pandanaceae disappeared from the
western and the Cyclanthaceae from the eastern hemisphere.

Herosiares.—This primitive series is very widely dis-
tributed and contains relatively few species, probably on
account of its aquatic character. Three of its families (Pota-
mogetonaceae, Naiadaceae, and Hydrocharitaceae) have a
world-wide distribution. The remaining five families are some-
what restricted as follows: Aponogetonaceae in the Indian
Ocean region, Triuridaceae in the tropics of both hemispheres,
Butomaceae extending from the tropics into temperate regions,
while Juncaginaceae and Alismaceae are mostly outside of the
tropics in the northern and southern hemispheres.

AraLes.—The possible relationship of this group to the pre-
ceding one has been mentioned. The aquatic Lemnaceae are
universally distributed, but 92 per cent of the Araceae are
within the tropics, being massed chiefly in South America,
India, and the East Indies. This family, as the palms, affords
a good illustration of the development of continental diversi-
ties. In this ease, however, the diversity has not reached so
extreme a stage as in the palms, in which even the tribes of
the orient and occident are for the most part distinct. Among
Avoids the tribes of the two hemispheres are by no means dis-
tinct, at least two tropical genera (Cyrtosperma and Homalo-
mena) have species in both hemispheres, and the monotypic
Pistia is found in every tropical region. The species are more
numerous in the American tropics, but the number of genera
is nearly twice as great in the oriental tropics. The Aroids
differ further from the palms in having at least six genera
characteristic members of north temperate vegetation, and these
for the most part are common to both hemispheres.

18

264 MORPHOLOGY OF ANGIOSPERMS

GeiumaLes.—The world-wide distribution of this great
alliance, from tropical to boreal conditions, has resulted in no
continental tribes, comparatively few continental genera, and
very numerous cosmopolitan species. So far as geographic dis-
tribution is concerned, it may well represent the primitive
stock from which the foilowing alliances have branched.

Farrnares.—This alliance is made up of a remarkable group
of isolated families, apparently being poorly adapted for cos-
mopolitan distribution. Only three of the eleven families have
a more extensive distribution than a hemisphere, Eriocaula-
ceae, the most cosmopolitan family, being massed in the tropics,
Comimelinaceae occurring everywhere except in boreal condi-
tions, and Pontederiaceae being represented in all warmer re-
gions. Four families (Flagellariaceae, Restionaceae, Centro-
lepidaceae, and Itapateaceae) belong to the southern hemi-
sphere, three (Mayacaceae, Xvridaceae, and Bromeliaceae) are
restricted to the western hemisphere, and Philydraceae are
Australian.

Liriares.—This series, in contrast to the Farinales, is made
up of characteristically cosmopolitan families. Liliaceae and
Iridaceae are literally cosmopolitan, Amaryllidaceae and Tac-
caceae are massed in all tropical regions, Juncaceae are best de-
veloped in the cool temperates of the northern and southern
hemispheres, Haemodoraceae are represented in tropical Amer-
ica and Australia, Stemonaceae are scattered in patches in
Australia, Asia, and North America, and Dioscoreaceae are
mainly tropical. Only Velloziaceae are restricted to a single
hemisphere, and the restriction is remarkable, since all of the
70 species are credited only to Brazil.

Serramryates.—The four families of this series are all
tropical, two of them (Musaceae and Zingiberaceae) being re-
stricted to the oriental tropics, and two (Cannaceae and Maran-
taceae) to the oecidental.

OrcimaLes.—The massing of orchids in the tropies of both
hemispheres is well known, but they are by no means restricted
to tropieal conditions. As a rule, the numerous tropical genera
are not only restricted to hemispheres, but are often very local;
while the temperate genera are represented in both hemi-
spheres, and the most northern genera even contain cosmopoli-
tan species.

GEOGRAPHIC DISTRIBUTION OF ANGIOSPERMS 265

Upon examining such data, certain generalizations in refer-
ence to the distribution of Monocotyledons become apparent.
These will doubtless be modified by a fuller knowledge of the
distribution of families, but they will serve to illustrate certain
facts:

1. Four great terrestrial families (Gramineae, Cyperaceae,
Liliaceae, and Iridaceae) of Monocotyledons are world-wide
in their distribution. This means that they have been able to
become adapted to every condition of soil and climate possible
to ppt ade vegetation.

The Monocotyledons include a remarkable number of
nee hydrophytie families which also have a world-wide dis-
tribution so far as fresh and brackish waters are concerned.
The families are Typhaceae, Potamogetonaceae, Naiadaceae
Hydrocharitaceae, Lemnaceae, and Pontederiaceae, four of
them belonging to the Helobiales. In spite of this wide dis-
tribution, these families contain less than 200 species. When
this fact is taken in connection with the 10,000 species belong-
ing to the four cosmopolitan terrestrial families mentioned
abe ve, it becomes evident that the very diverse conditions of the
land surface are far more favorable to the production of species
than the comparatively uniform aquatic conditions.

There is a decided massing of monocotyledonous families
in the tropics. This is so marked as to suggest that Monocotyle-
dons as a whole are essentially tropical.

As a corollary to the last statement, the entire absence
of boreal forms, excepting the few belonging to the families
of universal distribution, is noteworthy.

5. The poor representation of Monocotyledons in the
southern hemisphere, exclusive of the world-wide families,
is remarkable. Especially is this true of Australia, a region
prolific in endemic forms among Gymnosperms and Dicotyle-
dons.

Very few families are characteristic of temperate re-
gions, and these (Sparganiaceae, Juncaginaceae, Alismaceae,
and Juncaceae) are represented in both the northern and
southern hemispheres, and none of them are of the higher
petaloideous type.

The tropical representation of Monocotyledons is ap-
proximately equal in the two hemispheres, not merely in num-

266 MORPHOLOGY OF ANGIOSPERMS

ber of species but also of families. The tropical families repre-
sented in both hemispheres are Butomaceae, Triuridaceae,
Palmaceae, Araceae, Eriocaulaceae, Commelinaceae, Amaryl
lidaceae, Taccaceae, Dioscoreaceae, Burmanniaceae, and Orchi-
daceae. Those peculiar to the oriental tropics are Pandanaceae,
Aponogetonaceae, Musaceae, and Zingiberaceae. Those peculiar
to the occidental tropics are Cyclanthaceae, Mayacaceae, Xyri-
daceae, Bromeliaceae, Haemodoraceae, Velloziaceae, Canna-
ceae, and Marantaceae.

8. The great preponderance of epiphytic forms in the
American tropics is probably associated with the culmination
of the rainy forest. The two great epiphytic families are
Bromeliaceae and Orchidaceae, the former being restricted to
the occidental tropies, and the latter much more abundant there
than in the oriental tropics.

9. The peculiar distribution of the three genera of Stemona-
ceae is noteworthy and suggestive. Stemona, with four or five
species, ranges from the Himalayas to southern Australia.
Croomia has one of its species (C. pauciflora) in Florida, Geor-
gia, and Japan; while the other (C. japonica) is restricted to
Japan. The monotypic Stichneuron is restricted to the East
Indies. The occurrence of a single species of this oriental
family in Georgia and Florida, and that species native also to
Japan, is difficult to explain.

ARCHICIILAMYDEAE

It is impossible to consider the geographic distribution of
the Archichlamydeae in such detail as that of the Monocotyle-
dons. The series are so numerous and indefinite that a presen-
tation of their separate distribution would be confusing and
not very significant. An examination of available but very
insufficient data has resulted in the following extremely general
statements : i

1. No family has developed a world-vide distribution as
have several families of the Monocotyledons and Sympetalae.
It must be understood that this fact is related to the great
diversities in the group, that have resulted in the recognition
of numerous families. The family differenees recognized by
faxonomists are perhaps not to he pressed too far in any com-
parison of the geographic distribution of the three great ‘Angio-

GEOGRAPHIC DISTRIBUTION OF ANGIOSPERMS 267

sperm groups. If they are of equal value, the Archichlamydeae
respond more readily to geographic conditions than do the other
groups. We suspect, however, that they are of very unequal
value, and that the kind of response shown by the Archichlamy-
deae to changed conditions happens to concern the structures
used for determining families more than in the other groups.

2. Among the Archichlamydeae no distinetly boreal family
has been developed, as among the Sympetalae.

3. The great tropical family is the Leguminosae, by far
the largest Angiosperm family excepting the Compositae. If
the Mimosa forms are to be regarded as the primitive ones, it is
interesting to note that they are massed in tropical Africa and
Australia, and that it is the highly specialized Papilio forms
that have chiefly occupied the temperate regions.

4. Certain great families are characteristic of the north
temperate regions, usually being comparatively insignificant in
the tropics. These are the Polygonaceae, Caryophyllaceae,
Ranunculaceae, Cruciferae, Saxifragaceae, Rosaceae, Onagra-
ceae, and Umbelliferae.

5. As among the Monocotyledons, aquatic forms are com-
mon and cosmopolitan, but this habit does not characterize
whole families so frequently as in the former group. The fact
that the aquatic habit is found chiefly among the Monocotyle-
dons and Archichlamydeae must be associated with the fact that
in these groups the most primitive Angiosperms occur. The
cosmopolitan character of such forms may be illustrated by
the Ceratophyllaceae, which with only three species extends
from the arctic to the antarctic regions, occurring even in Aus-
tralia and the Fiji Islands.

6. There is a distinct pairing of continents especially in
tropical display, as was noted among the Monocotyledons, in
this case America usually being one member of the pair and
Asia or Africa the other. In this pairing, what may be called
the Pacifie-distribution, involving Asia, the East Indies, or
Australia on the one hand, and the Americas on the other, is
particularly prominent. For example, the Amarantaceae are
massed in Sonth America and the East Indies, the Lardiza-
balaceae in South America and southeastern Asia, the Calyean-
thaceae in North America and Japan, the Lauraceae in Amer-
ica and Asia, the Malvales chiefly in America and Asia, the

268 MORPHOLOGY OF ANGIOSPERMS

Myrtaceae in South America and Australia, ete. This pairing
is still more evident if closely related families are included, as
the Sarraceniaceae in North America and the Nepenthaceae in
tropical eastern Asia and the East Indies. The pairing of
Australia and Africa is less notable, as the Jimosa tribe, massed
in tropieal Australia and Africa, and the Thymelaeaceae, chiefly
oceurring in temperate Australia and the Cape region. The
pairing of America and Africa, or the Atlantic-distribution,
is quite rare.

7. The predominance of the American tropics in the devel-
opment of Archichlamydeae is marked, as might be inferred
from the last paragraph, almost all of the tropical groups being
represented there, and two great families (Cactaceae and Melas-
tomaceae) being alinost exclusively American.

8. As might be expected, there is a much greater display of
Archichlamydeae in the north temperate regions than in the
south. Two large families, however, are characteristic of the
south temperate regions—namely, the Proteaceae, chiefly Aus-
tralian, some South African, and a few South American; and
the Thymelacaceae, characteristic of Australia and the Cape

region.

9. It is of interest to note that the dominant tree-groups,
so characteristic of Archichlamydeae, are of different alliances
in the different regions. For example, in north temperate re-

gions the Juglandales, Fagales, ete., dominate; in the tropics

the Lauraceae are the characteristic tree-forms: while in south
temperate regions the Proteaceae are the prominent. archi-
chlamydeous forest trees.

10, There is a notable diffusion of types into all regions,
so that very few famihes are restricted in their representation,
although most of them have a fairly definite region of massing.
Characteristic tropical families have representatives in the tem-
perate regions, and families chiefly developed in the temperate
regions have tropical representatives.

SYMPETALAEB

The alliances of Sympetalae are comparatively so few and
well defined that they may he considered separately,

ERICALES.—This alliance is peculiar in contaiming distinet-
ly temperate and boreal forms. It includes an arctic fanuly

GEOGRAPHIC DISTRIBUTION OF ANGIOSPERMS 269

(Diapensiaceae), an Australian family (Epacridaceae), and a
great massing ot heath-forms in the Cape region.

PriuvraLes.—The three families are very distinct in their
geographic distribution, Myrsinaceae being tropical, especially
American, Primulaceae north temperate and boreal, and
Plumbaginaceae characteristically oriental in the halophytic
conditions of the Mediterranean and Caspian regions.

Esrnares.—The alliance is almost exclusively tropical, and
in both hemispheres.

GnrytranaLes.—The alliance as a whole is more largely
massed in the tropics through the tropical display of its largest
families, Apocynaceae and Asclepiadaceae. It contains also a
great liana group (Loganiaceae) characteristic of South Amer-
ica and Asia, and there is a pairing of Africa and Asia by
the Salvadoraceae. The Gentianaceae have almost a world-
wide distribution, but are notable in their numerous alpine
species.

TusirLoraLes.—This great series is in the main broken
up into fairly well-restricted areas, and the chief features of
their distribution may be stated as follows: The Labiatae are
world-wide in their distribution, being notably massed in the
Mediterranean region. The Borraginaceae and Scrophularia-
ceae are the great north temperate families. The Solanaceae
are everywhere in the tropics, extending into temperate regions
especially in America. The Convolvulaceae, Polemoniaceae,
and Hydrophyllaceae are characteristically American, the first
being chietly tropical, and the other two characteristic of west-
ern North America. The Gesneraceae belong to all regions
of the southern hemisphere; while the Verbenaceae, Nolana-
ceae, and Acanthaceae are notably in tropical South America.
There are also two Mediterranean families, the Orobanchaceae
and Globulariaceae. The pairing of South America and Asia
is shown in the display of Verbenaceae and Acanthaceae; and
of tropical Asia and Africa in the display of Pedaliaceae.

Prantracrnates.—The genus Plantago is cosmopolitan.

Rusrares.—The Rubiaceae are prominently tropical Amer-
ican; the Caprifoliaceae and Valerianaceae are north temper-
ate throughout both hemispheres; while the Dipsaceae seem
to be confined to the temperate regions of the eastern hemi-
sphere.

270 MORPHOLOGY OF ANGIOSPERMS

CaMpaNALEs.—The Cucurbitaceae are tropical; the Cam-
panulaceae belong to the north’ and south temperate regions,
with the lobelias as tropical representatives; the Goodeniaceae
and Candolleaceae are Australian; the Calyceraceae are mainly
tropical American; and the Compositae are world-wide in their
distribution.

The main conclusions to be derived from the above facts are
as follows:

1. The Sympetalae as a whole are better defined geograph-
ically than the Archichlamydeae. This probably follows from
the fact that they are better defined structurally.

2, There is a much more even distribution between the
tropics and temperates than among the Monocotyledons and
Archichlamydeae. Of course the tropical display is the larger,
but it is hardly more than might be regarded as the normal
ratio of inerease in passing from the temperates to the
tropics.

3. The Sympetalae as a whole, the youngest of the Angio-
sperm groups, seem to have become prominently adapted to the
relatively unoccupied temperate and boreal conditions, and to
have made in them their most characteristic display. From
this general point of view, the Monoecotyledons and Arehi-
chlamydeae are characteristically tropical, and the Svimpetalae
as characteristically temperate.

4. There is a remarkable paucity of aquatie forms as com-
pared with Monocotyledons and Archichlamydeae. This is
probably associated with at least two facts—namely, the lack
of primitive angiospermous types among the Sympetalae, and
the previous occupation of the water conditions by the older
Monocotyledons and Arehichlamydeae.

5. The Sympetalae show no such notable continental pair-
ing as is characteristic of the Archichlamydeae. Tt would seem
that this may be related to the temperate and boreal develop-
ment of the group, which would retain continental connections
much longer than would be possible for a group of more tropical
tendencies,

6. The dominance of America in the tropical display of
Sympetalae is almost as notable as among the Archichlamvydeae.
The excessive rainfall is doubtless one faetor in the explana-
tion, but whether it is the chief one is uneertain.

GEOGRAPHIC DISTRIBUTION OF ANGIOSPERMS 271

7. The sympetalous families of world-wide distribution are
the Compositae, Labiatae, and Plantaginaceae.

8. The great north temperate families are the Borragina-
ceae and Scrophulariaceae.

9. The characteristic boreal group is the Ericales, a group
that finds no parallel among the Monocotyledons and Archi-
chlamydeae.

CHAPTER XIV
FOSSIL ANGIOSPERMS

Tue importance of a knowledge of the ancient history of
Angiosperms can not be overestimated. The morphological
conclusions as to phylogeny that can be confirmed by historical
evidence rest upon the securest available foundation. Unfor-
tunately, the paleobotanical record of Angiosperms is very frag-
mentary and poorly understood. The published accounts are
dominated mainly by stratigraphy rather than by plant-groups,
and the named material is often so uncertain as to its athnities
that the morphologist is extremely perplexed in drawing any
couclusions. Even when all data are rejected excepting those
that rest upon reasonably secure botanical evidence, any con-
clusions must be extremely tentative, not only because much
of the evidence is negative, but also beeause much of the re-
jected material undoubtedly contains valuable testimony. In
spite of this uncertainty, it may be useful to put together such
testimony as we possess. Even this may modify some concep-
tions as to phylogeny.

MONOCOTYLEDONS

When the parallel venation of leaves was taken to be a dis-
tinctive character of the Monocotyledons their presence in the
Carboniferous was claimed. But since it has beeome known
that such leaves are equally characteristie of the great Paleozoic
group Cordaites, as well as of other Gymnosperms, and of cer-
tain heterosporous Pteridophytes, this claim rests wpon no sub-
stantial basis. So far as we have been able to examine the
testimony, it must be said that the existence of Paleozoic Mono-
cotyledons has not been proved,

There is no historiersl evidence that the Monocotyledons
have ever been a dominant race, as the Gymnosperms have

or
whe

FOSSIL ANGIOSPERMS 2738

been, and as the Dicotyledons now are, although they do not
seem to be so abundant now as they were during the Tertiary.
When they do appear in undoubted forms, they are almost com-
pletely differentiated and w idely distril buted. Their ancestral
forms are obscured in the maze of unintelligible forms that pre-
cede them. The only suggestion of paleobotany as to the origin
of the Monocotyledons is that they are certainly a younger type
than the Gymnosperms.

Rejecting the claim for Carboniferous Monocotyledons, we
encounter one for their existence during the Jurassic. This
rests upon the occurrence of certain forms of grass-like habit,
which suggest Monocotyledons, but such evidence can not be
accepted as conclusive. There is certainly no clear proof of the
existence of Monocotyledons in any strata earlier than the Cre-
taceous.*

The probability of Monocotyledons during the Jurassic rests
not upon positive discovery, but upon the fact that during the
Cretaceous they were abundant everywhere, and give evidence
ot their long presence. The earliest history of the group,
therefore, is an absolute blank, and we are introduced to it in
an advanced stage of development.

The record can be considered under three general catego-
ries—namely, (1) those families represented during the Cre-
taceous, (2) those whose earhest representatives are in the Ter-
tiary, and (3) those only known since the Tertiary. It must
be observed that the second and third categories are based upon
negative evidence—that is, representatives of these families
have not been found as yet at any earlier period. It must also
be remembered that many plants have a habitat and structure
unfavorable to their preservation as fossils, so that failure to
discover them in the geological series is no positive evidence
that they did not exist. With the uncertainties understood it
may be safe to present such evidence as we have.

Creraceous Fawitres.—There seems to be sure evidence
of the existence of five families during the Cretaccous, and a
possibility of the occurrence of a sixth.

The Pandanaceae were present and were widely distrib-

* See Sewarp, A. C.: Notes on the Geological History of Monocotyledons.
Annals of Botany 10: 205-220. pl. 14. 1896.

274 MORPHOLOGY OF ANGIOSPERMS

uted. This fact seems to substantiate the claim as to the primi-
tive character of this family, and to discount the theory of its
origin as a reduction type. Not only did the screw-pine exist,
but the family was richer in forms than at present, all the
living genera containing more numerous species than now, and
at least one extinct genus having been recognized.

A little later in the Cretaceous the Palmaceae occurred
abundantly, but in genera that are now for the most part
extinet. Their distribution was very wide-spread, remains hav-
ing been found in deposits from Greenland to Egypt. This
early association of Pandanaceae and Palmaceae is corrobora-
tive of the idea of their genetic relationship, and the later ap-
pearance of the Palmaceae further confirms the morphological
evidence that they may have been derived from the Panda-
naceae. ;

The Potamogetonaceae were abundant, a fact that coincides
well with their SE position as the most primitive
of the Helobiales, and controverts the idea that they are a
reduced type. That they were more abundantly displayed dur-
ing the Cretaceous than now is evidenced by the fact that the
majority of our present genera were represented, and at least
three extinct genera have been detected.

The above families would be expected by a morphologist to
oceur among the earliest Monocotyledons, but the Cretaceous
record also discloses the presence of the Liliaceae. However,
they are comparatively few i in number, oceur in the upper mem-
hers of the Cretaceous series, and do not fairly display them-
selves until the Tertiary, when numerous and now extinet gen-
era ann These earlier liliaceous forms are of the Smilax
type, but this negative evidence is very uncertain, as this type
is peeuharly favorable for preservation,

The Dioscoreaceae also appeared along with the Liliaceae,
and are so confused with the Smilax forms as to be diffeult
to disentangle.

The sixth family, whose existence during the Cretaceous is
possible but far from certain, is the Araceae, to which certain
doubtful forms have been referred, Tt may have been seantily
represented, and its asseeiation with the Potamogetonaceae
would be confirmatory of Eneler’s suggestion as to their genetic
econneetion, Fi

FOSSIL ANGIOSPERMS 2

Tertiary Famriies.—To the five monocotyledonous fami-
hes represented during the Cretaceous the Tertiary adds at least
fourteen, the older families also showing a largely increased
development. It will be interesting tc note how these addi-
tional families fill ont the ten great series of Monocotyledons.
In each case the Cretaceous representative is put in paren-
thesis.

1. Pandanales.—(Pandanaceae), Typhaceae, Spargania-
ceae. This primitive series is thus completed as at present
recognized,

2. [[elobiales.—(Potamogetonaceae), Juncaginaceae, Buto-
maceae, Hydrocharitaceae. This series is completed by the
appearance of its highest member, and the Butomaceae are
fairly representative of the Alismaceae.

3. Glumales.—Gramineae, Cyperacere. The occurrence of
grvass-like forms during the Jurassic has been referred to, but
the absence of grasses from the Cretaceous record seriously
militates against the claim that these Jurassic forms were
grasses. It is since the Tertiary that the Gramineae have be-
come most richly developed and widely spread, numerous ex-
tinct genera having been described. Although it would seem
impossible to determine the relationships of grasses from frag-
mentary material, and doubt must be expressed as to the rela-
tionships implied in such names as Poacites, Arundinites, etc.,
there is good evidence for the statement that the earliest grass
types were related to such tropical forms as Arundo, Phrag-
mites, Bambusa, ete.

4. Palmales.—(Palmaceae). The only family of the series
became much more largely developed and wide-spread during
the Tertiary.

5. Synanthales.—Cyclanthaceae. This family, the only
member of the series, appeared during the Eocene Tertiary,
and its early association with the serew-pines and palms con-
firms its supposed relationship to them.

6. Arales.—(Araceae?). The doubtful appearance of this
family during the Cretaceous has been mentioned, and this
claim is not helped by the fact that they are no better known
during the Tertiary. Sneh forms as do occur resemble Acorus
and Pistia. The so-called “ Protolemnas” seem too doubtful
to be included.

276 MORPHOLOGY OF ANGIOSPERMS

7. Farinales.—Restionaceae, Centrolepidaceae, Eriocaula-
ceae. Three of the eleven families of the series are thus intro-
duced, the first two now being restricted to the southern hemi-
sphere, but during the Tertiary ranging through Europe.

8. Liliales.—( Liliaceae, Dioscoreaceae ), Juneaceae, Lrida-
ceae, The last family is the highest member of the series, and
its appearance before certain of the lower families is altogether
doubtful.

9. Seitaminales.—Musaceae. ‘The series consists of four
families, and this one, now centined to the oriental tropics, is
recognized as the most primitive.

10. Orchidales.—N ot represented.

At the end of the Tertiary, therefore, there is reasonable
evidence as to the existence of all the great series of Monocoty-
ledons excepting the highest, and of nearly one-half the fam-
ilies.

DICOTYLEDONS

Any evidence as to the comparative antiquity of Monocoty-
ledons and Dicotyledons is much to be desired, but as yet the
historical evidence is not definite, for no undoubted Monocoty-
ledon has been recorded from strata older than those in which
typical Dicotyledons first oceur, and vice versa. The great and
sudden prominence of the Dicotyledons in the Upper Cretaceous
and Tertiary was long a puzzle, only reheved by the solitary
Populus primaeva of the Lower Cretaceous. Comparatively
recent studies, however, of contemporancous beds in the United
States and Portugal now regarded as Lower Cretaceous have
thrown much light upon the subject, and since 1888 our knowl
edge of the origin of the Dicotvledons has increased rapidly.
It should be remembered that the group is largely composed of
herbaceous plants, and could not have a fair representation
among fossil forms.

Lowrr Creraceous Dicoryiepoxs.—The dicotyledonous
flora of the Lower Cretaceous was an abundant one, and is of
erveat imterest in the history of Dicotyledons. Tt consists of a
plexus of forms, some of which are clearly related to existing
Dicotyledons, others are clearly Dieotyledons but with no living
representatives, while others are vague im their relationship to
Dicotyledons. The few forms that can be referred with any

FOSSIL ANGIOSPERMS 247

definiteness to modern groups are fairly submerged by the ex-
tinct and vague types. Such a plexus is consistent with any
evolutionary theory of the origin of Dicotyledons, and that it
has been definitely discovered in the Lower Cretaceous is of
great importance,

Proangiosperms.—These are the vague forms referred to
above as being not definitely Dicotyledons but suggestive of
them. They are recognized by stem-structure and leaf-vena-
tion, and seem to be related to numerous modern families,
being good illustrations of so-called “ comprehensive types.”
It is hardly to be doubted that many of them represent primi-
tive Dicotyledons. If the Lower Cretaceous be divided into
five periods, the Proangiosperms not suggestive of modern
eroups are the only dicotyledonous forms in the first. In
the other periods they also oceur, but in diminishing impor-
tance as compared with the increasing number of recognizable
forms. These clearly antecedent and for a time associated
forms are very suggestive of their significant relation to modern
Dicotyledons.

Forms suggestive of Modern Groups.—After the first period
of the Lower Cretaceous, forms suggestive of modern groups
appear. They are so clearly Dicotyledons as not to be included
among the Proangiosperms, but they are just as distinctly not
modern types. Their generic names suggest the modern resem-
blances, but these must not be taken to indicate relationships.
For example, such names as Leguminosites, Menispermites,
Myrsinophyllum, Proteophyllum, Peucedanites, ete., tell of cer-
tain superficial resemblances, but may be very far from indi-
cating real relationships.

Modern Genera.—As already stated, no modern genera were
associated with the Proangiosperms during the first period of
the Lower Cretaceous. In the second period, however, an ex-
tinct species of Populus has been recognized, the most ancient
living genus of Dicotyledons known. In the third period Mag-
nolia and Liriodendron are recorded; in the fourth Salix, Aris-
tolochia, Sassafras, Adoxa, and Aralia appeared; and in the
fifth Myrica, Laurus, Eucalyptus, and Viburnum are recorded.

Tn considering this record of the Lower Cretaceous the fol-
lowing things become evident:

1. The genera, so far as they are identical with living gen-

278 MORPHOLOGY OF ANGIOSPERMS

era, are practically all members of the Archichlamydeae. The
case of Viburnum, and even of Aralia, is peculiar, and perhaps
suggestive of a far more complete development of the Dicoty-
Iedons than the records have shown.

2. The early appearance of Populus confirms the general
primitive character of naked flowers and the anemophilous
habit.

3. None of the known chalazogamic forms are represented
in the above list, so that chalazogamy can hardly be regarded
as a primitive character, as has been claimed, unless it be as-
sumed that these earher genera were chalazogamic and later
a porogamic.

. Of the twelve modern genera represented in the list, no
less es an eight are recognized by morphologists as primitive
in char acter.

The occurrence of one of the Sympetalae in the upper-
most member of the Lower Cretaceous, and that an epigynous
form, needs explanation. It leads to at least one of three con-
clusions. Hither the determination is a mistake, or a large
representation of sympetalous genera remain to be discovered
in the Lower Cretaceous, or the present view as to the relative
rank and phylogeny of sympetalous families must be modified.
If the determination of Viburnum is the correct one, its associa-
tion with Aralia is confirmatory of a genetic connection which
we have long maintained.

6. That epigyny had appeared among the undoubted Archi-
chlamydeae during the Lower Cretaceous is seen by the exist-
ence of such a genus as Hucalyptus.

Upper Creraceous Dicoryitepons.—Much less is known
of the flora of the Upper Cretaceous than of the Lower Creta-
ceous. There must have been a large development of existing
genera, such as Salix, Populus, and Liriodendron being well
known, as well as an introduction of new ones

Tertiary Dicoryiepons.—The record aif the dicotyledo-
nous flora of the Tertiary is naturally made up of the trees and
shrubs. The forest display was evidently as extensive and va-
ried as now. In addition to the genera mentioned above, all of
which show increasing development, there appeared the Betula-
ceae, Fagaceae, Juglandaceae, Moraceae, Proteaceae, Berberi-
daceae, Staphyleaceac, Aceraceae, ete. ‘This means an almost

FOSSIL ANGIOSPERMS 279

complete display of the more primitive Archichlamydeae. A
notable introduction during the Tertiary was that of the Legu-
minosae. That these appeared first only as Mimosa forms is a
strong confirmation of the primitive character of this tribe, as
well as of its possible relation to the Rosaceae.

The above facts in reference to the early history of the Di-
cotyledons seem to warrant the following conclusions:

1. The modern Dicotyledons were derived from a plexus of
vague forms developed largely in the Lower Cretaceous and
known as Proangiosperms.

2. The Cretaceous and Tertiary display is almost exelu-
sively made up of Archichlamydeae, the dominant types being
the more primitive Archichlamydeae.

3. The Sympetalae are practically absent from the Creta-
ceous and Tertiary, and represent therefore a comparatively
recent type.

4. The possible appearance of Viburnum, associated with
Aralia, at the close of the Lower Cretaceous suggests a connec-
tion of Umbellales with the Sympetalae not recognized by tax-
onomists.

5. None of the highly specialized groups of the Archichla-
mydeae are represented in the Cretaceous and Tertiary, such a
family as the Leguminosae being represented by its most primi-
tive type, and all the types being what may he called “ compre-
hensive.”

6. The identity of genera in the eastern and western hemi-
spheres indicates the absence of continental diversities, which
later became so striking a feature in geographical distribution.

7. The theory that simple flowers are necessarily reduced
rather than primitive structures seems to have a complete refu-
tation in the testimony of history.

19

CHAPTER XV
PHYLOGENY OF ANGIOSPERMS

Tur phylogeny of any great group will probably always
remain a batting problem. At the same time, theories of phy-
logeny serve to coordinate knowledge and stimulate investiga-
tion. The phylogeny of Angiosperms is an unusually obscure
problem. The hypotheses proposed seem to include almost
every possibility, but thus far they have been more interesting
than convineing. When similarity of structure was taken as a
sure indication of genetic relationships, the problem promised
an approximate solution. But since it has been proved that
similar structnres may develop independently, the ditheulty of
solution has apparently become insurmountable. Under such
circumstances it is questionable whether a discussion of the sub-
ject is profitable, but a statement of the problem may not be
out of place.

The first phase of the problem has to do with the common
or independent origin of the Monoeotyledons and Dicotyledons.
It has been assumed generally that the two groups are mono-
phyletic. The chief argument, and in fact the only morpholog-
ical one for the monophyletic theory, les in the great wni-
formity of the peculiar development of both the male and
female gametophytes. It is argued that the independent
origin of such exact details of development and structure
is inconceivable, and this argument has been reenforeed re-
cently by the discovery in both groups of the peculiar phe-
nomenon called “ double fertilization.” The argument is cer-
tainly a very strong one, and yet there are rebutting proposi-
tions. Even such similarity in structure may be the natural
outeome of the changes that resulted in the evolution of seeds,
and these are now generally believed to have appeared in inde-

280

PHILOGENY OF ANGIOSPERMS 281

pendent lines. Again, the fundamental differences in the de-
velopment of the embryos of the two groups are hard to recon-
cile upon the theory of monophyletic origin. Add to this the
fundamental differences in the structure of the stem and in
the character of its vascular bundles, and the derivation of one
group from the other seems more inconceivable than the deriva-
tion of the Dicotyledons from the Gymnosperms. Still another
argument against the monophyletic theory is furnished by the
historical testimony. The Proangiosperms of the Lower Cre-
taceous, so far as known, appeared associated with undoubted
Monocotyledons, and merged gradually into recognizable Di-
cotyledons, without indicating any relationship to the Mono-
cotyledons. The emerging of Dicotyledons from this vague
group either indicates that Monocotyledons and Dicotyledons
originated independently, or that the Proangiosperms were
transition forms between Monocotyledons and Dicotyledons.
This latter alternative is in turn inconceivable, especially since
the most primitive Dicotyledons are recognized to be even more
primitive than any of the Monocotyledons.

Recently, however, the morphological arguments in favor
of the monophyletic origin of Angiosperms have been reen-
forced by anatomical investigations, which point to origin from
a common proangiospermous stock, or the derivation of the
Monocotyledons from the more primitive Dicotyledons. In the
following chapters it will be noted that on anatomical grounds
Jeffrey regards the Monocotyledons as strictly monophyletic
and modern, derived from the Dicotyledons or their parent
stock; and on the same ground Queva® thinks that the Mono-
cotyledons are derived from the lower Dicotyledons. In her
study of the origin of the cotyledon in Monocotyledons, Miss
Sargant 1* concludes that the Monocotyledons are a specialized
branch from the Dicotyledons. In Anemarrhena, one of the
Liliaceae, she finds two opposed vascular bundles in the ter-
minal cotyledon. These run down into the short hypocotyl,
where each divides into two, and the four phloems so formed
are continuous with those of the tetrareh primary root. This
suggests that two cotyledons are represented, which were sepa-
rate in some dicotyledonous ancestor. The same investigator
also finds in Hrianthis, one of the Ranunculaceae, a possible
illustration of this dicot edonous ancestor; for the petioles

282 MORPHOLOGY OF ANGIOSPERMS

of the cotyledons are united throughout their length, showing
two opposed bundles, as in the cotyledon of Anemarrhena.
Attention should be called to similar cotyledonary tubes in
Dicotyledons, and since nearly all of these are geophilous plants
Miss Sargant 7? has inferred that the fused condition of the
cotyledons in the monocotyledons has arisen in connection with
the geophilous habit. We herewith reproduce Miss Sargant’s
list of dicotyledonous seedlings with a well-marked cotyledonary
tube.

Anemone coronaria, A. alpina, A. blanda, A. narcissiflora, A. rupi-
cola, Ranunculus parnassifolius, Trollius Ledebouri, Erianthis hiema-
lis, Delphinium nudicaule, D. hybridum and vars., Aconitum Anthora,
Leontice vesicaria, L. altaica, Podophyllum peltatum, P. Emodi, Car-
damine spp., Oxalis spp., Rhizophora Mangle, R. conjugata, Megar-
rhiza californica, 8myrnium perfohatum, 8. rotundifolium, §. Olusa-
trum, Bunium luteum, Chaerophyllum bulbosum, Prangos ferulacea,
Serratula radiata, Dodecatheon Meadia, Polygonum Bistorta, P. sphae-
rostachyum, and Rheum Moorcroftianum.

Holm * has also studied the two completely united cotyledons
of Podophyllum, which suggested to him the possibility that
the “pair” may be regarded as a single cotyledon. In her
study of the “ monocotyledonous Dicotyledons,” Miss Sargant 7!
claims that the so-called single cotyledon is a fusion of two
cotyledons, special reference being niade to the well-known case
of Ranunculus Picaria. It may be noted also that in 1896
Delpino* urged the origin of the monocotyledonous De
from Dicotyledons through Butomus. Recently Hal lien? 20 /bas-
ing his phylogeny upon sporophylls and foliage leaves (* tro-
phophylls”), has urged the origin of Monocotyledons from
Dicotyledons, claiming that they have arisen from the region
of the Ceratophyllaceae and Ranuneulaceae.

There can be no question that among the Nvmphaeaceae,
Ranunculaceae, and Berberidaceae there occur anatomical strue-
tures very suggestive of Monocotyledons, as Campbell 1% has
recently pointed out, but that this proves the origin of Mono-
cotyledons from Diecotvledons rather than the reverse is not
evident. Even the evidence derived from cotyledons has been
taken by Lyon ™ as indicating that the dieotvledonous eondi-
tion has been derived from the eradual splitting of the single
cotyledon of Monoeotyledons. Tf the view of the phylogeny of

PHYLOGENY OF ANGIOSPERMS 283

the cotyledon maintained by Lyon!" be true (see Chapter IX),
the Monocotyledons are more primitive than the Dicotyledons
and have given rise to them.

It is an old view, however, that the Dicotyledons are the
more primitive, and that the Monocotyledons have been derived
from them as a reduction series. Later the relatively primi-
tive character of the Monocotyledons was maintained without
serious opposition. A detailed presentation of the phylogeny
ot ue ORpenn from this point of view may be found in
Bessey’s * ** Phylogeny and Taxonomy of the Angiosperms.’

In our judgment the evidence is strongly in favor of the
independent origin of the two groups, which have attained prac-

tica ily the same advancement in the essential morphological
structures, but are very diverse in their more superficial
features. Their great distinctness now indicates either that
they were always ‘distinct or that the ey originated from forms
that were really Proangiosperms and neither Monocotyledons
nor Dicotyledons. It may be well to state in this connection
that in speaking of the origin of one great group from another,
the former is not supposed to have arisen as a oe branch.
For example, to say that Monocotyledons have been derived
from Dicotyledons does not imply that a single monocotyled-
onous branch arose from some definite group of the Dicotyle-
dons, but that- probably several monocotyledonous lines arose
from one or more regions of the Dicotyledons, regions that
may or may not be illustrated by living groups.

‘The next phase of the problem raises the question whether
the Angiosperms have been derived from the Gymnosperms or
directly from the Pteridophytes. The general question is the
same whether one believes in their monophyletic character or
not. The older view is that the Angiosperms have been derived
from the Gymnosperms, and Gnetum has been regarded as the
nearest living representative of a transition condition between
Gymnosperms and Angiosperms. The argument is based upon
certain resemblances of Gnetum to the Angiosperms, chief
among them being the absence of archegonia, the organization
of eggs while the eametophy te consists of free cells, the presence
of a perianth and true vessels, and the Dicotyledon-like leaves.
This showing is strong but perhaps not conclusive. If this
origin be maintained, it is evident not only from the leaf char-

284 MORPHOLOGY OF ANGIOSPERMS

acters, but still more from the nature of the embryo and the
structure of the stem, that the primitive Angiosperm stock
would be the Dicotyledons. Strasburger recognized this neces-
sity when proposing the theory, and regarded the Monocotyle-
dons as a reduced branch from the Dicotyledons; which is
another reenforcement of the argument derived from recent
anatomical investigations. In fact, the Gymmosperm ances-
try of Dicotyledons also gains a point in the entire absence
of pteridophytie anatomical features in the shoots of Dico-
tyledons.

Lately, also, Karsten,!® in a morphological study of the
Jug] undlaneae, emphasizes their resemblances to Gymnosperms,
and concludes that the Angiosperms have been derived from such
forms as Gnetum. The historical argument against such a claim
is the absence of any certain evidence of the existence of Gretum
among the numerous Angiosperms of the Cretaceous and Terti-
ary. If it were related in any way to the origin of such a group as
the Angiosperms, it seems probable that it would have left some
evidence of its existence. Of course this is negative evidence,
and remains of ancient Gnetales may be found in the tropics
or in the southern hemisphere. The argument from the pres-
ence of a perianth is particularly vulnerable, since the so-called
perianth merely represents the bracts common among Gymno-
sperms, and the most primitive Dicotyledons and Monocotyle-
dons have no perianth. Further, the presence of true vessels
is an argument as much in favor of the origin of the Angio-
sperms from certain heterosporous Pteridophytes as from Gne-
tum. Although we regard the origin of Angiosperms from
Gymnosperms as very improbable, the embryo-sac structures
of (rnetum are suggestive of the way in which the character-
istic sac-structures of the Angiosperms may have arisen from
a compact gametophyte. This is all the more probable since
the sac-structures of certain Juglandaceae and of Peperomia
pellucida have been found to be suggestive of those of certain
species of Gnetim.

If the Gymnosperms are not the ancestral forms of the An-
giosperms, their direct derivation from the Pteridophytes be-
comes a matter of course. The Pteridophyte that has been most
persistently associated with the origin of Angiosperms is [soe-
fes. Its resemblances to the Monocotyledons have suggested

oS

PHYLOGENY OF ANGIOSPERMS 2

or

8:

that it may be the nearest living representative of their ancestral
forms. Lsoetes is a remarkably isolated group among the Pteri-
dophytes, with no clear affinities, so that its own connection with
the Pteridophyte stock is not evident. The most striking re-
semblance to Monocotyledons occurs in the embryo, in which
the single cotyledon is terminal and the stem-tip arises later
as a lateral structure. The development of the male gameto-
phyte resembles Angiosperms more than it does Gymnosperms,
while the female gametophyte is equally suggestive. However,
these gametophyte characters are shared by Selaginella. The
general habit and vegetative structure of [soetes hear some re-
semblance to those of an aquatic Monocotyledon, and the anat-
omy of the stem is suggestive of such forms as Yucca and Dra-
caena. There can be no question that the resemblances of [soe-
tes to the Monocotyledons are more numerous than those of any
other lving Pteridophyte. The most telling resemblance is
the character of the embryo, but the fact that its axis is trans-
verse to that of the suspensor is a serious obstacle. Campbell
has called attention to the fact, however, that in the embryos
of Lilaea subulata and Zannichellia the apex of the root is not
directed toward the suspensor but to one side, so that the axis
of the embryo is oblique to that of the suspensor. A possible
explanation of these laterally directed roots, however, is sug-
gested by Murbeck’s recent account of Ruppia (page 196), in
which a primary root is formed with the normal orientation,
but soon disorganizes, while a lateral root, formed very early,
is the first functional one. As between the Gnetum origin
of Angiosperms and the Isoetes origin of Monocotyledons the
latter view must be preferred. Such a view, of course, does
not imply that the present Monocotyledons have been derived
from the present Isoetaceae, but that the ancestral forms of
the two were probably genetically connected. If this be true,
doubtless Isoetes represents a reduced branch of some old stock
that gave rise to the more vigorous Monocotyledons. The only
possible alternative as to the origin of Monocotyledons, in case
they have arisen independently of the Dicotyledons, seems to
be to regard them as the end of a heterosporous line that
developed independently from the eusporangiate Filicales,
whose Pteridophyte members are extinct. Such an hypothesis
is only necessary in the event that those based upon known

286 MORPHOLOGY OF ANGIOSPERMS

structures prove to be insufiicient; but the problem seems to
have reached this contingency now.

To many, any conclusion as to the origin of the Monocoty-
ledons involves that of the Dicotyledons, which they would re-
gard as an ancient branch from the Monocotyledon stock. We
have already cited reasons why such a view does not commend
itself to us, and prefer to regard Dicotyledons as of independent
origin. If the two lines have a common origin, it seems to us
that the arguments in favor of the derivation of Monocotyle-
dons from the more primitive Dicotyledons are the more con-
vincing. Both lines to-day include very primitive forms, and
the structure of the flower and character of the megasporan-
giate archesporium are more primitive among existing Dicot-
yledons than among Monocotyledons. Whether Dicotyledons
represent an independent angiospermous line, as we prefer to
believe, or the primitive Angiosperm stock, it remains to dis-
cuss their possible origin. The fact that they emerged from
a primitive group called Proangiosperms, which was largely
developed in the first period of the Lower Cretaceous, seems
to be fairly well established by paleobotany. The question
thus concerns the origin of the Proangiosperms. They do
not seem to warrant the belief that they represent a common
stock from which both Monocotyledons and Dicotyledons have
been derived, for the Monocotyledons are believed to have ex-
isted in unmistakable forms before the large assemblage of Pro-
angiosperms gave rise to unmistakable Dicotyledons. Still
less conceivable is it that the Proangiosperms represent the
transition forms from Monocotyledons to Dicotyledons, for
nothing in their known structure seems to suggest such a view.
That they were derived from Gnetum-like forms is discredited
by the fact that there is no sure record of the existence of
Gnetum at such an early period, and to have given rise to
such an assemblage of forms it must have been a eonspienous
group.

If we turn to the earlier groups that were sufficiently prom-
iment and at all suggestive of having given rise to the Pro-
angiosperms, we encounter the Coniferales, Cyeadales, Lyeopo-
diales, and Filicales. The Gymmosperm-origin of Dicotyledons
seems to be most unlikely with the exclusion of Gnefum. At
the same time, it might be claimed that Dicotyledons represent

PHYLOGENY OF ANGIOSPERMS 287

an independent line from the Gymnosperm-stock, that advanced
in the same direction and much farther than did the Gnetum-
line. At the same time, all the essential morphology of the
Gymnosperms is less favorable to such an origin than is that
of the heterosporous Pteridophytes.

The Lycopodiales certainly deserve serions consideration in
this connection. The structures of Selaginella are xhout as
suggestive of Dicotyledons as those of Isoetes are suggestive
of Monocotyledons, the embryo being as distinctly dicotyledo-
nous as that of [soetes is monocotyledonous, and the seed-like
character of the megasporangium supplies a still more striking
resemblance. Such a view does not imply that the present com-
paratively modern genus Selaginella has given rise to the Pro-
angiosperms, but that the latter may have been derived from
the same ancient Lycopodium stock.

The only remaining alternative hypothesis is that mentioned
in connection with the origin of the Monocotyledons, namely, the
derivation of the Proangiosperms as an independent heteros-
porous line from the abundant ancient ensporangiate Filicales,
and this view is supported by anatomical testimony. It may
be that further knowledge of the Proangiosperms will help to
establish such an hypothesis.

It seems to us that the last two hypotheses deserve the most
consideration, as likely to include the future results of investi-
gation.

It should be noted in connection with the origin of Dicoty-
ledons that there is much evidence in favor of the view that they
include two independent lines. For example, Campbell inclines
to the view that one line is derived from the Arales, passing
by way of the Piperales and amentaceons groups to the isoear-
pous Sympetalae, while the other arises from the apocarpous
Helobiales, and by way of the Ranales and later groups cul-
minates in the anisocarpie Sympetalae. Although not inclined
to accept the origin suggested, the existence of two such inde-
pendent lines of Dicotyledons has very much in its favor,
whether derived from the Monocotyledons or not.

A summary of our present views, as developed in the preced-
ing pages, may be stated as follows: The Monocotyledons and
Dicotyledons represent two independent lines derived directly
from Pteridophyte stock, probably from the Filicales. At the

2388 MORPHOLOGY OF ANGIOSPERMS

same time, the arguments in favor of the monophyletic origin
of Angiosperms are strong; and if this view be accepted, the
derivation of Monocotyledons from primitive Dicotyledons
sees to rest on stronger evidence than the reverse relationship.
It must also be said that the Gymnosperm origin of Angio-
sperms is not to be discredited so much now as formerly.

The student of the phylogeny of any group of vascular
plants should be acquainted with certain general theoretical
views. Among them the origin of the sporophytic generation
is one of the niost fundamental. Two theories are under dis-
cussion, known as that of homologous origin and that of anti-
thetic origin, names applied by Celakovsky. According to the
former theory, the sporophyte is the lineal descendant of the
sexless individuals common among Thalophytes and homolo-
gous with the sexual individuals; according to the latter the-
ory, the sporophyte is a new structure intercalated in the life
history of plants and holding no phylogenetic relation to any
preceding individuals. The theory of homologous origin is re-
ferred to Pringsheim in 1876; that of antithetic origin was
formulated by Celakovsk¥ in 1877, but was presented in detail
by Bower in 1890. In 1896 the theory of homologous origin
was again brought into prominent notice by Scott in a presi-
dential address before the British Association; and two years
later Bower, upon a similar occasion, defended the theory of
antithetic origin. A general presentation of the subject by
Klebs,* Lang,’ and Hartog * followed, including the testimony
of recent investigations. Undoubtedly the strongest argument
in favor of the homologous origin of the sporophyte is derived
from the phenomena of apogamy and apospory; and among
Ferns these have been coming to light so rapidly and are in-
duced so readily that the powers of gametophyte and sporo-
phyte, at least in this group, seem to be easily interchangeable,
a fact most easily explained by their homologous character. It
will be noted that in all this discussion there is no suggestion
that sporophytes may have arisen in both of these ways, a possi-
bility that will be considered a little later.

One of the most suggestive theories of recent years is
Bower's! theory of the strobilus. No better statement of its
main points can be made than that of the author himself in
his summary.

PHYLOGENY OF ANGIOSPERMS 289

1. Spore-production was the first office of the sporophyte, and the
spore-phase has constantly recurred throughout the descent of the
Archegoniatae ; the spore-bearing tissues are to be regarded as primary,
the vegetative tissues as secondary, in point of evolutionary history.

2. Other things being equal, increase in number of carpospores is
an advantage; a climax of numerical spore-production was attained
in the homosporous Vascular Cryptogams.

3. Sterilization of potential sporogenous tissues has been a wide-
spread phenomenon, appearing as a natural consequence of increased
spore-production.

4. Isolated sterile cells or layers of cells (tapetum) served in many
cases the direct function of nourishing the developing spores, being
themselves absorbed during the process.

5. By formation of a central sterile mass (columella, etc.) the spore-
production was, in more complex forms, relegated to a more superficial
position.

6. In vascular plants, parts of the sterile tissue formed septa, par-
titioning off the remaining sporogenous tissue into separate loculi.

7. Septation to form synangia, and subsequent separation of the
sporangia, are phenomena illustrated in the upward development of
vascular plants.

8. Such septation may have taken place repeatedly in the same
line of descent.

9. The strobilus as a whole is the correlative of a body of the
nature of a sporogonial head, and the apex of the one corresponds to
the apex of the other.

10. Progression from the simpler to the more complex type de-
pended upon (@) septation, and (b) eruption to form superficial appen-
dicular organs (sporangiophores, sporophylls) upon which the sporan-
gia are supported.

11. By continued apical growth of the strobilus, the number of
sporophylls may be indefinitely increased.

12. The sporophylls are susceptible of great increase in size and
complexity of form ; in point of evolutionary history, small and simple
sporophylls preceded large and complex ones.

13. In certain cases foliage-leaves were produced by sterilization
of sporophylls.

This theory means that the leafy sporophyte is derived from
such a sporophytic structure as is displayed by the sporogonium
of Bryephytes; but, as suggested by Klebs and Lang, it may
have had an entirely independent origin, and may have no
phylogenetic connection with such a structure as a sporogonium.
This view, together with its possible relations to the question
of antithetie versus homologous origin of the sporophyte, has

200 MORPHOLOGY OF ANGIOSPERMS

been discussed by Coulter,® the substance of whose paper may
be stated in the following extracts:

It has been common to regard the distinct sporophyte as having
been established once for all by the Bryophytes, and the sporophytes
of the higher groups to have been derived from those of the Bryo-
phytes. In searching for the origin of the leafy sporophyte, therefore,
attention has been focused upon the sporogonia of Bryoplhytes. ...
The doctrine that any plant structure, however important, can have
but one phylogeny, is hardly tenable at present... . In contrasting
the sporophytes of Bryophytes and Pteridophytes, they seem to have
nothing in common except that they are usually derived from the
oospore and represent an asexual generation. These facts are im-
portant, but so are the numerous other facts in which they differ
sharply. ...

It may be well to contrast the leafless and leafy sporophytes. In
the former case the structure is never independent of the gametophyte,
develops no lateral members, has nothing comparable to sporangia,
and its whole tendency is to render complex the spore-producing
region. In the latter case the sporophyte is dependent upon the game-
tophyte only in its embryonic stage, develops prominent lateral mem-
bers, has distinct simple sporangia, and its whole tendency is to render
complex the sterile or nutritive tissues. As one traces the evolution
of the Bryophyte sporogonia they give evidence of increasing com-
plexity and hence rigidity, and little promise of originating such a
diverse tendency as that shown by the sporophyte of Pteridophytes.
... The origin of leaves on the gametophore of mosses suggests that
leaves may develop in response to more favorable conditions for their
work, and such development may result in the great reduction of
chlorophyll work done by the less favored region, and its consequent
simplification. It is evident that with the exchange of an aquatic for
a terrestrial habit the thallose body would not be a favorable type for
chlorophyll work, and that the development of chlorophyl1 tissue upon
erect structures of various kinds might follow. Among Bryophytes
the erect structure laid hold of is the gametophore, and not the sporo-
gonium. ...

In considering whether it is possible to disregard the Bryophytes
in our search for the origin of the leafy sporophyte, we are largely
influenced by the fact that the Bryophyte sporophyte, throughout its
whole history, is dominated by a tendeney which does not appear in
the Pteridophyte sporophyte. Before the establishment of alternate
generations the plant body may be said to have had three functions,
namely, chlorophyll work, and the production of gametes and spores.
The appearance of the Bryophyte sporogonium was dominated by the
separation of spore-formation from the other functions, chlorophyll
work being retained by the gametophyte, along with gamete-produc-

PHYLOGENY OF ANGIOSPERMS 291

tion. Attention has been focused so long upon the gametes and spores
as the two dominant factors in differentiation that it is hard to con-
ceive of the possibility of the domination of another factor. It is
entirely conceivable, however, that another form of differentiation
may have occurred, dominated by the needs of the chlorophyll work,
and not by spore-production. Certainly a great need for change, when
aquatic conditions were exchanged for terrestrial, was in connection
with the display of chlorophyll tissue. It would seem as if the Bryo-
phytes had laid emphasis upon spore-production, and therefore never
became organized for the fullest use of terrestrial conditions, while the
Pteridophytes laid emphasis upon chlorophyll work and became highly
organized for terrestrial life. It would seem possible, therefore, with
the three factors to take into account, that two distinct asexual lines
may have been organized, distinct in the factor selected to domi-
nate.

If more favorable structures can be developed in response to the
needs of spores or gametes, there seems to be no good reason why more
favorable structures may not be developed in response to the needs of
chlorophyll work. If such a response in structure is possible, it would
naturally express itself first in developing the largest display of chlo-
rophyll tissue in the most favorable region of the body, which would
gradually become differentiated more and more distinctly from the
rest of the body. It does not seem clear why the appearance of an
erect leafy axis, bearing neither gametes nor spores, is not quite as
supposable as the appearance of a sporophore with neither gametes nor
leaves, or a gametophore with neither spores nor leaves. . . .

With such an origin of the leafy sporophyte, it would follow that
foliage leaves are not secondary but primary structures, and that sporo-
phylls have arisen from the differentiation of foliage leaves bearing
sporangia, a state of things certainly suggested by the most primitive
Pteridophytes known. It would further follow that the evolution of
the strobilus has followed the development of foliage leaves, a view in
accordance with the older morphology. Such a view would make
intelligible the great “ gap ” recognized as existing between Bryophytes
and Pteridophytes, as the two groups would not be phylogenetically
connected, and would have developed along very divergent lines from
the first. It would mean that at least two independent sporophyte
lines have appeared, the Bryophyte line probably with an antithetic
origin, and the Pteridophyte line possibly with an homologous origin.
The great prominence of the latter line, with its Spermatophyte
sequence, is correlated with the development of a vascular system, and
it would seem as though the evolution of an elaborate vascular system
must have depended upon the domination of chlorophyll work.

Knowledge of the various theories as to the origin of species
is so much a part of the essential training of the morphologist

292 MORPHOLOGY OF ANGIOSPERMS

that no résumé of the subject is necessary. Until very recently,
the various theories involve the idea that a species is produced
as the cumulative result of slight variations through successive
generations. In sharp contrast to this De Vries has recently
proposed what is called the mutation theory, a brief statement
of which may be of service. The experimental work that fur-
nishes a substantial basis for the theory was conducted with
Angiosperms, and a special student of the group should be pre-
pared to recognize any testimony for or against it. A suggest-
ive feature of the work of De Vries is his attempt to break
away from the speculative method and to subject the problem
to experimental investigation. Whether his results indicate a
general method of the origin of species in nature or an ocea-
sional method, or are capable of an entirely different expla-
nation and hold no relation to the normal origin of species,
remains for future work to determine. In any event, the theory
will stimulate investigation and deserves consideration.

The occasional sudden appearance of what have been called
“sports”? is well known, but they have not been prominently
associated with the origin of species. They have been referred
to as cases of “ saltatory evolution,’ and in 1864 WKolliker

‘

seems to have been responsible for the term ‘ heterogenesis ”
as apphed to this phenomenon. Quite independently and sim-
ultaneously De Vries"? and [Xorschinsky !* have elaborated the
same theory as to the origin of species, the former calling it
the “ mutation theory,” the latter using Koélliker’s name * hete-
rogenesis.” _Xorschinsky has brought together a mass of data
from the records of gardeners and horticulturists to show that
most ot the culture “ varieties ” have arisen through heterogene-
sis rather than by selection. De Vries, on the other hand, has
experimented extensively with Gnothera Lamarchiana, a spe-
cies showing mutability in a high degree. This American spe-
cies was found naturalized on an area in Holland about 1875,
and afterward spread rapidly. When observed by De Vries,
in 1586, two new species were detected among the normal forms,
and they have maintained themselves ever since. From 1886
until the publication of his book, De Vries made observations
upon the naturalized areas and carried on cultures in the botan-
ical garden at Amsterdam. As a general result, it mav be stated
that out of 50,000 seedlings of G2. Lamarchkiana 800 were mu-

PHYLOGENY OF ANGIOSPERMS 293

tants. Of these 800, about 200 were the new species named
(i. lata; that is, the same new species appeared about 200
times. Various other new species appeared, and were preserved
by culture. The mutants also occurred in every direction in
the same environment, showing no indication of being responses
to external conditions. In the great majority of cases the mu-
tants were constant from the outset, there being no development
and fixation of characters through selection, and no transition
between parent and offspring. Experiments with other species
seem to indicate that the majority of species are at present
immutable, varying within certain narrow limits, but not giving
rise to mutants.

Solms-Laubach?° has shown that in all probability Cap-
sella Heegert has arisen in this way from C. Bursa-pastoris ;
and Carlson '* has suggested a similar origin for certain Swed-
ish forms of Succisa pratensis; while Jordan’s work with Draba
verna has discovered about 200 immutable forms within the
old species limits, that probably represent true species derived
by mutation from a parent of great mutability.

The experiments of De Vries seem to indicate that there is
a definite limit to individual variability, beyond which selection
can not go. Furthermore, it is claimed that selection never fixes
a character, but reversion may occur after any number of gen-
erations of culture. In short, natural selection can not create
anything new, but can modify within definite and narrow lim-
its; while mutation brings into existence something new, which
will continue as a new species if it can survive the struggle for
existence. There is thus drawn a sharp contrast between muta-
bility and ordinary variability, the latter being governed by
environment, the former independent of it. Hence, while most
species are immutable, all are more or less variable.

At its present stage such a theory can not be accepted or
rejected. Either alternative will demand a vast amount of care-
fully sifted experimental evidence. It should be remembered
that the subject lends itself readily to observations that are
really inferences, and a vast amount of data will doubtless be
forthcoming that can not be regarded as testimony. The stu-
dent of Angiosperms, however, is in a position to encounter
useful data, for the group 1s a very modern one and seems to
contain many mutable species. It should further be remem-

204 MORPHOLOGY OF ANGIOSPERMS

bered that the whole theory is based upon the present concep-
tion of species, a conception so variable that it can not be
defined. Furthermore, although there may be a fixed limit
to ordinary variation, there must also be a fixed limit to the
extraordinary variation called mutation, and this remains to be
detined. In fact, there is evidence that extreme mutation re-
sults in functional derangement of organs, and the result is a
monstrosity, which may be regarded as an impossible new spe-
cies. Finally, even if mutation be found to explain the origin
of many new species, it does not follow that other processes
also may not be working to the same result.

In a recent paper, Strasburger '? takes occasion to diseuss
the origin of species, taking the view that the results of natural
selection have been overestimated, and that new species have
arisen through mutation, due to internal causes alone, and
through * use and disuse,” by means of which a certain amount
of adaptation to environment is secured. To him the only func-
tion of natural selection appears to be to remove the less valu-
able forms produced through mutation and “use and disuse.”
Tt follows that the ordinary physiological operations do not
result in species, but affect them after they have appeared, and
that the origin of species is a morphological rather than a phys-
iological problem.

LITERATURE CITED

1. Bower, F.O. A Theory of the Strobilus in Archegoniate Plants.
Annals of Botany 8: 843-365. 1894.

2. DELPINO, F. Applicazione de nuovi criterii per la classificasione
dele piante. Mem. Real. Acead. Sci. Bologna V. 6: 83-116.
1896; see review Bot. Centralbl. 67: 370. 1896.

3. Bessey, C. E. Phylogeny and Taxonomy of the Angiosperms.
Bot. Gazette 24: 145-178. 1897.

4. KLERS, G. Alternation of Generations in the Thallophytes. An-
nals of Botany 12: 570-583. 1898.

5. Lane, W. H. Alternation of Generations in the Archegoniates.
Annals of Botany 12: 583-592. 1898. :

6. Harrog, M. Aiternation of Generations. Annals of Botany 12:

593-594, 1898.
. Houm, THEO, Podophyllum peltatum: a Morphological Study.
Bot. Gazette 27: 419-433. figs. 10,.1898.

8. CovLtter, J. M. The Origin of the Leafy Sporophyte. Bot.

Gazette 28: 46-59, 1899,

10.

ab

20.

21.

PHYLOGENY OF ANGIOSPERMS 295

. QUEVA, C. Contributions a l’anatomie des Monocotyledonées. I.

Les Uvulariées tubereuses. Lille. 1899.

SotMs-LavuBacH, H. Cruciferenstudien. 1. Capsella Heegeri
Solms, eine neue entstandene Form der deutschen Flora. Bot.
Zeit. 581: 167-190. pl. 7. 1900.

De Vries, H. Die Mutationstheorie, Versuche und Beobachtungen
iiber die Entstehung von Arten im Pflanzenreich. Vol. I. Leip-
zig. 1901. See reviews: Biol. Centralbl. 21: 257-269, 289-305.
1901; Bot. Centralbl. 87: 170. 1901; Bot. Gazette 33: 236. 1902.
Also The Origin of Species by Mutation, Science 15: 721-729.
1902.

2. KORSCHINSKY, 8S. Heterogenesis und Evolution. Ein Beitrag zur

Theorie der Entstehung der Arten. Translated from the Russian
by S. Tschulok. Flora 89: 240-363. 1901; also review in Bot.
Gazette 33: 396. 1902.

3. CaRLson, G. W. F. Ett par afvikande former af Succisa praten-

sis. Bot. Notiser 1901 : 224-226.

. Lyon, H.L. Observations on the Embryogeny of Nelumbo. Minn.

Bot. Studies 2: 643-655. 1901.

. CAMPBELL, D. H. On the Affinities of Certain Anomalous Dicot-

yledons. Amer. Nat. 36: 7-12. 1902.

. Karsten, G. Ueber die Entwickelung der weiblichen Bliithen

bei einigen Juglandaceen. Flora 90: 316-333. pl. 12. 1902.

. Lyon, H. L. The Phylogeny of the Cotyledon. Postelsia 1901:

55-86. 1902.

. SarGant, ErHeu. The Origin of the Seed-leaf in Monocotyledons.

New Phytologist 1: 107-113. pl. 2. 1902.

9, STRASBURGER, E. Ein Beitrag zur Kenntniss von Ceratophyllum

submersum und phylogenetische Erérterungen. Jahrb. Wiss.
Bot. 87: 477-526. pls. 9-11. 1902.

Hauer, H. Beitriige zur Morphologie der Sporophyle und des
Trophophylls in Beziehung zur Phylogenie der Kormophyten.
Jahrb. Hamburgischen Wiss. Anstalten 19: 1-110. 1902.

Saraant, Ergey. A Theory of the Origin of Monocotyledons,
founded on the Structure of their Seedlings. Annals of Botany
17: 1-92. pls. 1-7, 1903.

CHAPTER XVI

COMPARATIVE ANATOMY OF THE GYMNOSPERMS AND
THEIR ALLIES *

Tue skeletal structure of vascular plants has in the past
been used for phylogenetic purposes to a much smaller extent
than that of the higher animals. During recent years, however,
important advances in our knowledge of the anatomy of fossil
plants have made it apparent that the primary fibrovascular
skeleton of the vascular plants is even more conservative than
their reproductive organs, and consequently of great impor-
tance in arriving at the relationships of the larger groups. The
most extreme ecological conditions, acting for long periods, seem
to have little effect in modifying the essential features of the
primary fibrovascular framework, so that, for example, the
extremely xerophytic cactus and the hydrophytie water-lily
have exactly the same type of skeleton from the standpoint of
comparative anatomy. It sometimes happens, however, that
the woody framework is extremely complex in the adult. Re-
cent investigations which cover the whole field of living vascular
plants make it clear that the study of the development of the
sporeling or seedling provides a satisfactory key to the inter-
pretation of the most intricate skeletal strnetures of maturity.

A brief account of certain general results of recent anatom-
ical and developmental research in the case of the vascular
plants is accordingly necessary for an understanding of those
skeletal features of the Gymnosperms and their allies which
are of phylogenetic importance.

PTERIDOPHYTES

The simplest type of stem in the Pteridophytes is that in
which there is present a single pithless fibrovascular conductive

* Contributed by Professor Edward C. Jeffrey, of Harvard University.
296

COMPARATIVE ANATOMY OF GYMNOSPERMS 297

strand embedded in the parenchyma of the fundamental tissue.
Part of a transverse section of such a stem is seen in Fig. 108, A.
In the center is the concentric fibrovascular bundle or stele,
which consists of a mass of xylem completely surrounded by
phloem. The stele or central cylinder is bounded in turn by
brown sclerenchymatous fundamental tissue. This type of
stem, since it is a very primitive one, may conveniently be
called ‘ protostelic” (Jeffrey 1°).

Another common condition of the stem is seen in Fig. 108,
B, which represents a cross-section of the rhizome of Adiantum
pedatum. In this case the central cylinder is not a solid fibro-
vascular strand as in the preceding example, but a hollow cyl-
inder filled with fundamental tissue like that external to the
stele. The plane of section is just above the point of origin of
a leaf-trace, which may be distinguished as the smaller of the
two concentric masses of fibrovascular tissue. At a higher level
the gap in the cauline central cylinder closes, and the stele be-
comes circular instead of crescentic in cross-section. Similar
gaps appear above all the outgoing leaf-traces, and as a conse-
quence the central cylinder is essentially a concentric fibrovas-
cular tube, with gaps in its walls corresponding to the leaf-
traces. The type of central cylinder which has just been de-
scribed may appropriately be termed “ siphonostelic” (Jef-
frey 1°).

Fig. 108, C, is from a photograph of the adult stem of
Pteris aquilina, the common bracken fern. In this case there
are numerous concentric fibrovascular bundles present in the
fundamental tissue of the rhizome, and accordingly stems of
this type have been designated by Van Tieghem “ polystelic.”
It has been shown, however, that in such stems as are exempli-
fied by P. aquilina the primitive condition of the central cyl-
inder is a stelar tube with foliar lacunae (Jeffrey?*). Fig.
108, D, from the young stem of P. aquilina, sufficiently demon-
strates the truth of this statement. The young stem gradually
passes into the condition represented in Fig. 108, C, first by
the foliar gaps becoming so long as to overlap, and second by
the derivation of the large central strands from the inner wall
of the primitive stelar tube. Consequently the stem of P. aqut-
lina may be regarded on ontogenetic grounds as siphonostelic
and essentially similar to that of Adiantum pedatum.

298 MORPHOLOGY OF ANGIOSPERMS

Fig. 108, #, shows a type of central cylinder which at first
sight appears very like that of the adult stem of Pleris aqui-
lina; above on the right is a gap im the tubular stele, which
in this case corresponds to a branch. Laterally, on the left,
a foliar trace is to be seen in the fundamental tissue. The leaf-
trace is very small, and there is no gap in the central cylinder
corresponding to it. As in P. aquilina, there are two medullary
fibrovascular strands. It has recently been shown (Jeffrey 1% 1)
that in certain great groups of plants foliar gaps are constantly
present, while in other great groups they are unfailingly ab-
sent. The type of tubular stele characterized by the presence
of foliar gaps has been called “ phyllosiphonic,” and that pos-
sessing only gaps for the branches or ramular lacunae ‘ clado-
siphonic.” These distinctions are extremely constant, and con-
sequently of great phylogenetic value.

Fig. 108, F, is from a photograph of a cross-section of the
central cylinder of Osmunda Claytoniana. It is of special in-
terest because it is obviously of the same type as the central
eylinder of the Lying Gymnosperms, viz., a ring of collateral
bundles surrounding a medulla and separated from each other
by medullary rays. Van Tieghem* regards this type of stele
as derived by dilatation from the prostostehe condition, with
the formation of pith and medullary rays from the stelar pa-
renchyma. According to this view, the pith and rays are mor-
phologically different from and have nothing in common with
the fundamental tissue surrounding the stele.

Fig. 109, G, shows the forking of the central cylinder of
Osmunda cinnamomea. In this example the pith is obviously
continuous with the external cortex, and a strand of the very
characteristic brown selerenchymatous tissue of the cortex is
passing down into the medullary parenchyma through the gap
between the divisions of the fork. It is to be noted further
that the phloem passes inward around the divisions of the fork
for a considerable distance, and the endodermis is as well
marked on the inside as on the outside of the crescentic zones
of bundles. In Fig. 109, /7, there appears a not unusual econ-
dition of the central cylinder in O. cinnamomea. Unlike 0.
Claytoniana, there is present an internal endodermis along the
inner margin of the bundles, and the medulla is often charac-
terized by the presence of a mass of brown sclerenehyma similar

COMPARATIVE ANATOMY OF GYMNOSPERMS 299

to that which constitutes the external portion of the funda-
mental tissue of the stem,

Fig. 109, J, shows a central cylinder of Osmunda cinna-
momea, Where not only an internal endodermis is present but
also internal phloem as well. In Fig. 109, J, a part of the
wall of the same central cylinder is shown more highly mag-
nified. The sieve-tubes are easily recognized as large, appar-
ently empty elements. It has been suggested by Jeffrey 1° and
Faull,** as a result of the study of the anatomy of the whole
order, that the type of central cylinder found in the Osmunda-
ceae is the result of reduction from a siphonostelic condition
with internal phloem. This view of the matter is strengthened
by the fact that brown sclerenchyma is sometimes found in the
pith of Osmunda regalis and Todea barbara, although in these
species there is no longer any communication between pith and
cortex in the region of forking. Moreover, exactly similar
series of degeneration to that supped by the Osmundaceae
have been shown to exist in the case of certain polypodiaceous
ferns. Hence it may be assumed, in the present connection,
that the type of central cylinder exemplified by the Osmunda-
ceae has arisen by degeneracy from the siphonostelie type with
internal phloem; and that the medulla often shows signs of its
origin by striking histological resemblance to the cortex, even
when there is no longer any communication between the med-
ullary and cortical fundamental tissues.

Fig. 109, AY, shows the structure of one of the tracheary
strands of Osmunda cinnamomea. The protoxylem or primi-
tive wood appears as a cluster of small elements, just external
to a mass of wood-parenchyma. The protoxylem does not abut
immediately on the pith, as in the seed-plants, but is separated
from it by a considerable amount of wood-parenchyma and me-
taxylem; most of the metaxylem, however, les external to the
protoxylem. This type of tracheary bundle is very character-
istic of the ferns, and has been designated “ mesarch.”

Tn the case of the Lycopodiales, the tracheary bundle is of
still another type. If Fig. 108, #, be examined, it will be seen
that on the left of the central cylinder, opposite the leaf-trace
in the cortex, is a cluster of protoxylem. The primitive wood
in this case is external and next the phloem. This feature is
very characteristic of the Lycopods and their allies. Bundles

300 MORPHOLOGY OF ANGIOSPERMS

of the type just mentioned have been designated by Scott ®
“exarch.” Hence it may be stated that the bundles of the Fern-
like plants are characteristically mesarch; that the Lycopods
and their allies have exarch bundles; and that the prevailing
type in the Spermatophytes is the endarch bundle, the primitive
wood here coming next the medulla. These anatomical distinc
tions, however, are less trustworthy than those depending on
the presence and absence of foliar gaps, for many Ferns have
endarch bundles, while some (Lygodium, ete.) have even exarch
tracheary strands; on the other hand, Phylloglossum, a recog-
nized Lyecopod, has distinctly mesarch cauline bundles. There
are no known examples, however, of siphonostelic Lycopods
(Jettrey ?°) with foliar gaps, or of siphonostelic Ferns without
them.

CYCADOFILICES

Recently Potonié! has established a group, the Cycado-
filices, to include a number of fossil forms which are neither
true Ferns nor typical Gymnosperms, but which possess to a
large degree anatomical features of both alliances. These forms
can now be more advantageously discussed after the general
anatomical account presented in the foregoing paragraplis. The
vegetative anatomy of the Cycadofilices is of special importance,
both because of our entire ignorance of their reproductive or-
gans at the present time and because their anatomical structure
presents such an interesting transition from the pteridophytic
to the gymnospermous type.

Heterangium.—Fig. 109, L, taken from Scott’s admirable
Studies in Fossil Botany, shows the structural features of the
stem of Heterangium Grievii, a primitive representative of the
Cycadoftilices. The central evlinder is obviously protostelie and
very sumilar to that of Gleichenia flabellata of Fig. 108, A.
A striking difference, however, is the presence, on the outside
of the pithless primary wood, of a narrow zone of secondary
wood which is clearly distinguishable by reason of the regular
radial arrangement of its elements. In the cortex may be seen
leat-traces and groups of sclerotic cells. The external cortex
is bounded by a very characteristic hypodermal zone, which in
transverse section appears to be made up of alternating stripes
of parenchymatous and sclerenchymatous cells. Viewed longi-

COMPARATIVE ANATOMY OF GYMNOSPERMS 301

tudinally, the hypoderma is seen to be composed of a tangential
network of sclerenchymatous fibers having the meshes filled
with parenchyma.

Medullosa.—F ig. 110, M, reproduces a diagrammatic trans-
verse section of the stem of Medullosa anglica. On the outside
of the stem can be distinguished the same curious hypoderma
which is characteristic of the genus briefly described above.
The central cylinder in this case, however, is obviously not pro-
tostelic, but polystelic. Each of the large fibrovascular strands
is characterized by the presence of a considerable zone of sec-
ondary wood, which is indicated in the diagram by radiating
lines. There are no sclerifications in the cortex; but numerous
mucilage ducts, similar to those of the Marattiaceae and the
Cycads, may be seen in the fundamental tissue, both outside and
between the large fibrovascular strands, although their occur-
rence in the latter position is not shown in the diagram.

Very often the arrangement of the bundles in species of
Medullosa was much more complex than that appearing in Fig.
110, If. It has been shown recently that in ferns with even
the most complex arrangement of the bundles in the adult, by
following the development it is possible to arrive at the simple
stelar tube as a starting-point (Jeffrey ’’). It is consequently
extremely probable that the bundle system of the Medullosae is
to be regarded as primitively siphonostelic, like that of Pteris
aquilina.

In Fig. 110, NV, is represented a cross-section of a part of
the stem of Medullosa Solmst. Here are to be seen numerous
bundles, some of which are broad and plate-like and others
small and rounded in outline. The broader bundles are known

‘plate-rings,” and the smaller ones as “ star-rings.” An
interesting feature of the outer plate-rings is the fact that the
zone of secondary wood on the external face of the bundles is
often very much thicker than that on the internal face. This
peculiarity is especially well marked in old stems of JI. stellata.

Lyginodendron. —Fig. 110, O, taken from Williamson and
Scott,® reproduces admirably the general features of structure
of the stem Lyginodendron Oldhamium. On the outside is
the same curious hypodermal layer which occurs in Heteran-
gium and Medullosa. There is present also a zone of periderm
external to the fibrovascular tissues. In the cortex may be seen

302 MORPHOLOGY OF ANGIOSPERMS

clusters of sclerenchymatous tissue. These are also found in
the foliar gaps and in the pith. In the case of Lyginodendron
the primary wood is comparatively poorly developed and occurs
as distinct islands along the margin of the medulla. The sec-
ondary wood is characterized by the regular radial seriation of
its elements and is abundant, but, in ecmmon with many other
fossil Pteridophytes with secondary growth, shows no indica-
tion of annual rings. The continuity of the woody zone is
completely interrupted at intervals by the foliar gaps which
subtend the outgoing leat-traces.

Fig. 110, P, is a photograph of part of the ligneous zone
ot L. Oldhamium. The protoxylem, distinguished by the small
size of its elements, is seen to be embedded in the primary wood.
Most of the primary metaxylem lies on the medullary side of
the protoxylem, and a smaller portion between it and the sec-
ondary wood. Hence the primary bundle is mesarch, as is often
the case in the Ferns and their allies. Another important fili-
cinean feature is the presence of well-marked fohar gaps.

Fig. 110, Q, taken from Williamson and Scott,® shows an
interesting departure from the usual state of affairs in L. Old-
hamium; a primary wood-bundle is present, and external to it
is the usual secondary wood. In this case, however, there is
secondary wood and phloem on the medullary side of the bundle
as well. The condition represented in the figure is quite un-
usual in L. Oldhamium; but, as has been shown by Seward, is
of common occurrence in LZ. robustum. The facts just described
are of particular interest, because Scott © has made a specific
comparison between the central evlinders of Lyqinodendron and
Osmunda; and indeed, if we imagine a secondary zone of wood
present in the latter genus and the primary wood-bundles cor-
respondingly reduced m size, the resemblance becomes very
close. The occurrence of internal phloem and secondary wood
is paralleled by the discovery of internal phloem in OQ. cinna-
MOoMed,

The forms described above sufficiently illustrate the variety
of structure in the stem of the Cyeadofilices, and it now be-
comes necessary to discuss their phylogenetic significance. First
of all is to be noted the faet that they represent the three types
of stelar structure deseribed at the beginning of the chapter:
Heterangium being protostelie like Gleichenia: Medullosa sipho-

COMPARATIVE ANATOMY OF GYMNOSPERMS 303

nostelic ike Adiantum pedatum and Pteris aquilina; and Lygi-
nodendron siphonestelic, without internal phloem, as is gener-
ally the case in Osmunda, but resembling this genus in the ocea-
sional occurrence of internal sieve-tissue. The only striking
anatomical difference between the cycadofilicinean forms de-
scribed above and the parallel cases from the ferns lies in the
absence of secondary growth in the latter. This feature is now
known to be of minor importance, although great weight was
attached to it by the Brongniartian school of paleobotanists.

In regard to the particular type of the Cycadofilices which
gave rise to the Gymnosperms there is some difference of opin-
ion. Potonié,® 14 Worsdell,!® 17 and Jeffrey ?® consider the
Cycads to be derived from MJedullosa-like ancestors through a
Lyginodendron-like phase, by the gradual disappearance of the
internal secondary wood, and the final suppression of the cen-
tripetal primary wood. Scott,® 1° on the other hand, regards
Lyginodendron as the ancestral type, and as derived directly
from Heterangium by the formation of an intrastelar pith, and
not from medullosan ancestors by reduction. He further con-
siders the Medullosae to constitute merely a side branch of the
phylogenetic tree, and expresses the opinion that “we should
involve ourselves in unnecessary complications if we endeay-
ored to derive the simple primary structure of the cycadean
stem from the more elaborate organization of a Medullosa.”
However, examples of phylogenetic progression from the com-
plex to the simple are not at all uncommon. Striking illustra-
tions of this principle are afforded by the derivation of the
simple hyoid bone of the mammals from the complex hyoid
apparatus of the lower vertebrates, and the evolution of the
monodactyl horses of the present day from their four-toed an-
cestors of the Eocene. The histological structure of the medulla
in Lyginodendron strikingly resembles that of the cortex in the
presence of sclerotic nests, and this feature indicates strongly
community of origin of the medullary and cortical tissues.
Further, the occasional occurrence of internal phloem and in-
ternal secondary wood in Lyginodendron can most easily be ex-
plained as a vestigial relic of a siphonostelic condition, in which
internal phloem was normally present—i. e., a Medullosa with
a single series of bundles.

In regard to the special pteridophytic ancestry of the Cyca-

3804 MORPHOLOGY OF ANGIOSPERMS

dotilices there now seems to be little doubt. Scott has pointed
out that their fern-like foliage and usually mesarch bundles
indicate strongly a filicinean as opposed to a lyeopodinean ori-
gin. It has further recently been shown that they are phyllo-
siphonic (Jeffrey 1°), and since this feature is quite exclusively
characteristic of the ferns, it seems impossible to derive the
Cycadotilices from the Lycopods, as has been done by Renault.*

CYCADALES

The leaves and fern-like habit of the Cyeads afford good
external evidence of their filicinean origin, and their multicili-
ate sperms point in the same direction. The strongest evidence
of their having come from the ferns, however, is supplied by
their fibrovascular anatomy.

Fig. 111, R, is from a photograph of a cross-section of the
stem of Zamia floridana. Both pith and cortex are occupied,
as in Medullosa, by numerous mucilage ducts. In the cortex
several curved lines are present, which represent the curved
course of the foliar traces and are known as ‘ girdles.” AL
though some years old, the fibrovascular zone is quite narrow,
and shows no evidence of annual rings, a feature of resemblance
to the Medullosae and Lyginodendron.

In Fig. 111, S, the central cylinder of the same species is
shown more highly magnified. Its continuity is obviously
broken by gaps, which subtend the outgoing leaf-traces. The
mucilage duets of the medulla join with those of the cortex
through the foliar gaps. The central evlinder of Zamia, which
is quite typical of the Cycads in this respect, is consequently
phyllosiphonic. The mucilage ducts of the Cveads do not pene-
trate into the leaf-traces or root-steles. Hence it may be as-
sumned that, as in the Marattiaceae and Medullosae, they are
characteristic only of the extrastelar fundamental tissue. The
pith of the Cyeads, which contains mucilage duets continuous
with those of the cortex, is to be compared, therefore, with the
mucilaginous medulla of one of the Marattinceae or of a Wedul-
losa, and is to be regarded as extrastelar.

The foliar traces of the Cyeads are quite unique in strue-
ture and of considerable phylogenetic importance. The first
complete deseription of them was given hy Mettenius.t. As has
already been pointed out, the course of eyeadean leaf-traces is

COMPARATIVE ANATOMY OF GYMNOSPERMS 305

peculiar; for, instead of passing directly from the central cyl-
inder into the leaf, they usually pursue a circular course, so
that they reach their corresponding leaf on the opposite side of
the stem from their point of origin. In Zamia I have observed
this arrangement of the traces even in the seedling; but in
C'ycas, according to Mettenius,! the leaf-traces of the young
plant at first pursue a direct course, although at a later stage
girdles are present. During their cortical course the foliar
traces often undergo more or less complex anastomoses. The
structure of the strands in the cortex, and even in the base of
the petiole, is often concentric.

Fig. 111, 7, is from a photograph of a cortical bundle of
Cycas revoluta. The center of the bundle is composed almost
entirely of the large tracheids of the primary wood, which is
surrounded by the radially arranged secondary wood and
phloem. Higher up, in the lower part of the petiole, the bun-
dles lose most of their secondary wood and assume mesarch
structure. This is well seen in Fig. 111, U, which may be
compared with Figs. 109, K, and 110, P. A striking feature
of the bundle at this stage is that the primary wood is mostly
centripetal, and has consequently a markedly cryptogamic ap-
pearance. ,

Before discussing further the significance of the peculiar
structure of the foliar traces of the Cycads, it will be con-
venient to refer to an interesting discov ery made by Scott.*
Mesarch bundles have been found by him in the central cylinder
of the peduncle of the cone of Stangeria paradoxa and certain
other Cycads. The conservatism of reproductive organs is rec-
ognized by the universal use made of them in botanical classi-
fication. It is Scott’s opinion that in the conservative repro-
ductive branches (i. e., cones) of certain living Cycads the an-
cestral type of bundle is retained. Hence he believes that the
cauline central cylinder of the more or less remote ancestors
of the living Cycads must have had a structure similar to that
of the stem of Lyginodendron. This hypothesis is borne out
by the fact that the course of the leaf-traces in the cones of
Cyeads is the same as in the seedling of the genus C'ycas, and
in the vegetative stems of the extinct group of Cyead-like Ben-
nettitales; for they pass directly into the leaves (sporophylls)
and do not form girdles. Jeffrey 1° has pointed ont a similar

806 MORPHOLOGY OF ANGIOSPERMS

conservatism in the structure and course of the bundles in the
cones of Hguisetum.

Leaf-traces are likewise extremely conservative in structure,
for where cenogenetic modifications are present in the ordinary
cauline strands, the primitive type of fibrovascular bundle is
often retained in the leaf-traces, as well as in the reproductive
axis and in the seedling. Ancestral features are retained more-
over in the leaf-traces, especially those of the cotyledons, long
after they have disappeared elsewhere. Hence it is assumed
that the mesarch structure of the fohar bundles of the Cyeads
supplies a further argument for their derivation from ances-
tors like Lyginodendron.

The fact that cycadean leaf-traces are often concentric in
the lower part of their course has been used as an argument
by Worsdell?® in favor of the hypothesis that the cauline bun-
dles of the ancestors of the Cyeads were originally concentric.
This argument seems to have the same force as the similar argu-
ment in the case of the mesarch collateral bundles; and the fact
that concentric strands are comparatively rarely present in the
living Cyeads is probably due to the concentric condition being
further in the phylogenetic background. The structure of the
conservative tracheary strands of the leaves and peduncles of
the Cycads would seem to point to a more immediate ancestry
with the general organization of Lyginodendron, derived in
the remoter past from forms like Medullosa.

BENNETTITALES

The external vegetative features and the reproductive organs
of this interesting group have already been dealt with in the
companion volume tre eating of Gymnosperms (p. 142). Al-
though their reproductive organs differ very strikingly from
those of any living Cyeads, the fil brovaseular anatomy of the
Bennettitales is strikingly eyeadean (Scott). They possessed
a large eyeadean pith penetrated by mucilage canals and bound-
ed by a thin fibrovaseular ring. The continuity of the fibro-
vascular zone was broken at intervals opposite the large leaf-
traces, which separated in the cortex into ares of bundles pass-
ing directly into the leave The direct course of the foliar
bundles is to be compared ee that present in the cones only
of living Cyeads. This condition js probably to be regarded

COMPARATIVE ANATOMY OF GYMNOSPERMS 307

as ancestral, because it occurs also in cycadean seedlings. The
foliar iories of the Bennettitales were characterized by the
same peculiarities as those of the more medern Cyeads.

CORDAITALES

On page 135 of the companion volume treating of Gymno-
sperms, the reproductive features and general inarphulony of
this interesting alliance are sufliciently described. The central
evlinder of the Cordaites enclosed a large pith, and was charac-
terized by considerable secondary growth. Like the Cycads and
unlike the Conifers of the present “day, the secondary wood gen-
erally showed no annual rings. The wood of Cordaites, in some
cases at least, is to be identified with Araucarioxylon and Da-
doxvylon, fossil woods which occur as far down in the strata as
the Devonian. Scott!* has shown that in some species of
Araucarioxylon the primary wood of the stem was mesarch.
In a good many cases, however, the primary cauline bundles
of Cordaites are only distinguished by exceptionally large de-
velopment as compared with those of the higher living Gymno-
sperms. The leaf-traces were mesarch like those of the Cycads,
and Scott 1° compares the structure of a cordaitean leaf to that
of a pinna of Zamia. Fig. 111, V, shows the structure of a
transverse section of part of a lee a a species of Cordaites.

The organization of the cauline and foliar bundles of the
Cordaites favors the view of their derivation from a pterido-
phytic ancestry quite as much as that of their reproductive
organs. Their well-marked foliar gaps and their large leaves
clearly indicate their filicinean affinities. The thickness of the
woody cylinder and the freely branching habit of the Cordaites
indicates a greater proximity to the Coniferales than to the
Cyeadales.

GINKGOALES

The discovery of multiciliate sperms in Ginkgo is good evi-
dence for the antiquity and the affinities of the group. Still,
its pteridophytic features have suffered very considerable re-
duction as compared with the Cyeadales. Evidences of mesarch
structure are accordingly comparatively scanty. The bundles
of the stem are throughout endarch, and even the leaf-traces
show slight traces of the presence of centripetal wood. Wors-

308 MORPHOLOGY OF ANGIOSPERMS

dell, however, has found that the bundles of the cotyledons
show fairly well-developed cryptogamic wood. Fig. 111, W,
taken from Worsdell, makes the truth of this statement appar-
ent. The anatomical evidence leads to the conclusion that we
have in Ginkgo a comparatively modern genus as compared with
the living representatives of the cyeadean stock. Distinct foliar
gaps are present, which, taken together with the large leaves
and the multicilate sperms, point strongly to a filicinean an-
cestry.

CONIFERALES

The Coniferales are the prevailing Gymnosperms of the
present day, and it is not surprising that they should present
few anatomical features which can be considered ancestral.
Their usually small acicular leaves offer a striking contrast
to the large fern-like foliar organs of the older gymnospermous
groups. On account of the peculiar appearance of their foliage
it is not to be wondered at that they should have been associated
by Renault,? Campbell,® and Potonié 1? with lyeopodineous an-
cestors. Recent work on the anatomy (Jeffrey }%) of vascular
plants in general appears to show that in the case of the Conife-
rales the microphyllous habit has merely an ecological interest ;
for, unlike all the Lycopodiales, they have well-marked foliar
gaps in their cauline woody cylinder.

The researches of Worsdell § on the foliar bundles of the
Conifers have resulted in a clear demonstration of striking
pteridophytice features. Fig. 112, VY, represents a cross-section
of the cotyledonary bundle of Cephalotarus drupacea. On the
lower side of the fibrovaseular strand centrifugal wood, such
as is ordinarily present in the bundles of the Conifers, can be
made out. On the upper side of the bundle are large, thick-
walled elements, which are to be compared with the centripetal
tracheids of the eyeadean bundle in Fig. 111, U. Fig. 112, Y,
shows a longitudinal section of a cotyledonary bundle of C.
Fortunei, On the left are some pitted tracheids of the second-
ary wood. In the center of the bundle is the disorganized pro-
toxylem, while on the right is a single retienlated tracheid of
the ancestral centripetal wood. The ecotvledonary bundles of
Cephalotacus are consequently mesarch like those of the ordi-
nary leaves in Cyeads, but show striking signs of degeneracy

COMPARATIVE ANATOMY OF GYMNOSPERMS 309

in the centripetal cryptogamic wood. On the flanks of the
bundle the centripetal wood is continuous with the short-pitted
cells of the “ transfusion tissue” discovered by Frank in 1864.
In the bundles of the adult leaves of most of the living Con-
iferales there are only the very slightest traces of centripetal
wood. Worsdell has reached the interesting general conclusion
that the “transfusion tissue which occurs almost universally
in the leaves of gvymnospermous plants as an auxiliary con-
ducting system has been phylogenetically derived from the
centripetally formed xylem of the vascular bundle.”

Fig. 112, Z, shows the topography of a cross-section of a
branch of Thuja occidentalis. The leaves in this species are
extremely reduced, especially those occurring on the upper and
lower sides of the flattened branches. It might naturally be
expected that under these circumstances the foliar gaps would
be obscure or absent, but such is not the case, for subtending
the traces, which pass to the specially small leaves on the upper
and lower sides of the flattened branch, are two distinct foliar
lacunae. An examination of a large number of Conifers, some
with a very considerable xerophytic reduction in the size of
their leaves, has shown that the presence of foliar gaps is quite
constant in the group (Jeffrey 7%). It is now known that foliar
gaps are unfailingly absent in the tubular central cylinder of
living and fossil Lycopodiales and Equisetales, while on the
other hand they are invariably present in the Filicales. Hence
it may be assumed that the Coniferales, much as they resemble
the Lycopods in external appearance, are really derived from
filicinean ancestors by adaptation to a xerophytic mode of life.
The microphyllous habit is obviously a cenogenetic adaptation,
for the structure of the fibrovascular skeleton plainly indicates
that the coniferous stock is palingenetically megaphyllous, and
thus allied to the Ferns.

Fig. 112, AA, shows the structure of the root of Pinus
Strobus. The cortex and phloem surround a considerable mass
of secondary wood, in the center of which may be distinguished
the exarch primary wood. This feature is more clearly seen
in Fig. 112, BB, which represents the center of the section
shown in Fig. 112, AA, more highly magnified. It is an in-
teresting fact, to which Van Tieghem* has drawn attention,
that the mode of growth of the primary wood is the same in all

310 MORPHOLOGY OF ANGIOSPERMS

the vascular plants, viz., exarch and centripetal. The root of
the Spermatophytes is consequently conservative, and retains
intact ancestral pteridophytic features. It seems phylogenet-
ically significant that the exarch type of wood, so typical of
the Lycopods and their allies, is always present in roots, and
never the mesarch type so characteristic of the Fern-alliance.
This feature probably indicates that the Lycopod stock is an
extremely old one, a conclusion borne out by the fact that the
Lycopsid series had already culminated in the Carboniferous
age. It appears also not improbable that the Pteropsida, large-
leaved fern-like plants, took their origin from the microphyl-
lous lycopodinean stock in remote antiquity, and still exhibit
a trace of their origin in the primary structure of their roots.

GNETALES

This group is generally regarded as the highest of the Gym-
nosperms, a view which is borne out both by a consideration
of its anatomy and its reproductive organs. The latter show
in the case of Tumboa and Gnetum a considerable advance
toward the condition of true flowers, and this advance is paral-
leled by a reduction in the amount of female prothallial tissue
antecedent to fertilization. The Gnetales on the anatomical
side show indubitable evidence of gymnospermous relationship,
in the presence of quite typical foliar transfusion tissue. They
are distinguished anatomically from all other Gymnosperms,
however, living or fossil, by the presence of rudimentary vessels.

Fig. 113, CC, shows the structure of the wood in Gnetum
Gnemon. The secondary wood in this species consists of tra-
cheids and vessels, the latter heing easily distinguished by their
larger size. In some eases the fact that direct communication
between two contiguous vessels is merely the result of the dis-
appearance of the membrane of a bordered pit can be made
out.”

* For list of literature cited see end of Chapter XVII.

CHAPTER XVII
COMPARATIVE ANATOMY OF ANGIOSPERMS *

Tue question of the relationship of the two great divisions
of the Angiosperms has for many years been a matter of dis-
pute. Anatomically the differences between the Dicotyledons
and Monocotyledons are sutticiently well marked, but it has
not been easy to decide from ordinary anatomical data which
should be regarded as having the more primitive and antece-
dent organization. There can be little doubt that the two groups
are closely related, for in addition to the striking general re-
semblance of their sporophytic tissues there is almost an identi-
cal organization of the male and female gametophytes. The
Monocotyledons have by some been regarded as primitive on
account of the absence of a cambium in their ordinarily closed
bundles. This view has been strengthened by statements as to
their appearing earler in the geological strata than the Dicot-
yledons. It is now known beyond doubt, however, that many
of the earlier eryptogamous groups had well-marked secondary
growth, so that the absence of cambial activity is by no means
necessarily a primitive feature. Further, a more careful study
of plant fossils has made it clear that many of the remains for-
merly considered to be Monocotyledons are in reality Pterido-
phytes or Gymnosperms. Discussion of these interesting prob-
lems will be more profitable after the salient features of the
anatomy and development of the Angiosperms have been de-
scribed.

DICOTYLEDONS

It has been shown by Jeffrey * that the primitive condition
of the central cylinder in the Angiosperms is siphonostelic.
The tubular central cylinder of the seedling of Ranunculus,

* Contributed by Professor Edward C. Jeffrey, of Harvard University.
21 311

3812 MORPHOLOGY OF ANGIOSPERMS

for example, is characterized by foliar gaps such as are found
in the Filicales and Gymmosperms. Often in the seedling of
this genus there is present an internal liniting layer of the
stelar tissue which degenerates in the adult. Hence it may be
assumed, in the absence of negative evidence, that the pith of
Ranunculus belongs to the same morphological category as the
cortex. Matié, from a comparative study of the anatomy of
all the Ranunculaceae, has reached the conclusion that the genus
Ranunculus is the starting-point from which all the other gen-
era of the order have been derived. It follows apparently that
the central cylinder of the Ranunculaceae in general is suscep-
tible of the same interpretation as that of Ranunculus. Lf the
central eylinder of the Ranunculaceae be siphonostehe with
fohar gaps, i. e., phyllosiphonic, it may fairly be asswned
that the central cylinder of Dicotyledons in general is to be
similarly interpreted, especially as foliar gaps are universally
present, even in such extreme cases of xerophytie reduction as
Casuarina and the Cactaceae.

There are some instances of the occurrence of concentric
bundles in the Dicotyledons, but they appear to be of ceno-
genetic origin, and consequently of no phylogenetic importance ;
for in the cases which have been investigated, the concentric
condition is ordinarily absent in the seedling, the leaf-traces,
and the reproductive axes. This feature is illustrated by Pri-
mula farinosa, in which the bundles of the seedling, the repro-
ductive axis, and the leaves are always collateral; whereas those
of the older vegetative stem are usually concentric. Similar
phenomena have been observed in the Nymphaeaceae, Halo-
raghidaceae, ete.

In the older subterranean stem of Ranunculus acris the
fibrovascular tube becomes broken up into a series of segments
or bundles by the overlapping of the foliar gaps; quite often
in the stouter subterranean axis of Ranunculus acris. (Jet-
frey ™) the foliar bundles tend to run in the pith before passing
out to the leaves, thus offering a striking feature of resemblance
to the normal course of the leaf-traces in the Monocotyledons.
In the aerial stem, however, this feature is not present, as may
be seen in Fig. 113, DD, in which the arrangement of the
Iundles shown is the typieal one for the Dieotyledons. There
are a good many exceptions to the rule, however, e. g., Podo-

COMPARATIVE ANATOMY OF ANGIOSPERMS 318

phyllum, Gunnera, the Nymphaeaceae, ete. In the last-men-
tioned cases, the study of seedlings shows that the circular dis-
position of the fibrovascular strands is primitive. In Podo-
phyllum the scattering arrangement of the bundles is present
only in the aerial stem, and is absent in the rhizome, as well
as in the seedling.

Fig. 115, EL, is from a photograph of one of the bundles
of Ranunculus acris. The bundle is surrounded by a scleren-
chymatous sheath, which is thickest externally. The xylem
and phloem are separated from one another by a narrow zone
of cells arranged in radial rows, indicating that a sheht but
unmistakable cambial activity is present. The bundle is con-
sequently an open one. The protoxylem is obviously the inner-
most part of the primary xylem, so the bundle is endarch. En-
darch fibrovaseular strands with secondary growth by means of
a cambium are characteristic of the Dicotyledons. In aquatic
Dicotyledons (e. g., the Nymphaeaceae), however, secondary
growth is frequently absent.

The tracheary tissue of Dieotyledons with considerable sec-
ondary growth shows a further division of labor over the highest
Gymnosperms. In the oak, for example, there are thinner and
thicker-walled tracheids as well as vessels. The latter have
practically lost their water-conducting function and have very
few extremely small pits in their walls. They have thus been
differentiated for the purpose of support. In the beech this
division of labor ameng the tracheids does not take place, for
all the tracheids are of the same type and have well-developed
bordered pits in their walls. Strasburger? is of the opinion
that the wood-fibers of the Cupuliferae throughout are modified
tracheids, and hence merit the name of fiber-tracheids. Such
fibers are present in a number of the dicotyledonous orders.
Tn other cases, according to Strasburger, the wood-fibers are to
be regarded as derived from wood-parenchyma and not from
tracheids. In these instances they may properly be called libri-
form fibers. Tt is not clear, however, that a sharp distinction
can always be drawn between the two sorts of wood-fibers.

The sieve-tissue of the Dicotyledons is also more highly
specialized than that of the Gymnosperms, for the sieve-tubes
have special accessory cells. These accessory cells are derived
from the same mother-eells as the sieve-tubes, and are known

314 MORPHOLOGY OF ANGIOSPERMS

as companion cells. Companion cells are quite absent in the
Gymnosperms, but Strasburger has pointed out that here the
marginal cells of the medullary rays perform the physiological
function of companion cells.

The Dicotyledons as a group are distinguished anatomically
from the Gymnosperms by the entire absence of palingenetic
pteridophytie features of any sort in the fibrovascular tissues
of their stems and leaves. The bundles are throughout endarch
collateral, except in the root, where they are exarch, as in all
other vascular plants. The concentric bundles which oecasion-
ally occur in the Dicotyledons are obviously cenogenetic, and
have no phylogenetic significance. Both the xylem and phloem
of the Dicotyledons show a marked advance in differentiation
over all the Gymnosperms. The central cylinder of the stem
in the Dicotyledons is characterized by the presence of foliar
gaps, and accordingly, if the Dicotyledons are to be regarded
as derived ultimately from pteridophytie ancestors, as appears
to be the case, their descent is apparently from the Filicales,
either directly or through some living or extinct phylum of the
Gymnosperms. The argument for descent from a gymnosper-
mous ancestry seems to gain great force from the entire absence
of pteridophytice features in the shoot or leaves of the dico-
tyledonous Angiosperms.

MONOCOTYLEDONS

The arrangement of the bundles in the adult stem of the
Monocotyledons is very characteristic. Instead of being dis-
posed in a cirele, as in the Dicotyledons, they are scattered
throughout the central eylinder. Fig. 113, FF, illustrates this
pecuharity. Not infrequently, however, e. ¢., in the Lilia-
ceae, the bundles are obviously segments of a fibrovascular tube,
Just as is typically the ease in the Dicotyledons. Fig. 113, GG,
shows this feature in the rhizome of Clintonia borealis. Sub-
tending gaps between the bundles are to be seen smaller fibro-
vascular strands, which are leaf-traces. In this exainple we
have obviously to do with a fibrovaseular tube with foliar gaps.
Interestingly enough, the tubular arrangement of the fibrovas-
cular clements is frequently present in monocotyledonous seed-
lings, although characteristically absent in the adult. Hence
it may be interred that the tubular central eylinder with foliar

COMPARATIVE ANATOMY OF ANGIOSPERMS 315

gaps is the ancestral condition in the Monocotyledons. In some
cases, e. g., Symplocarpus foetidus, the pith and cortex are
continuous in the seedling through the foliar gaps, although
they no longer appear to be so in the adult. An internal endo-
dermis or stelar boundary is also sometimes present in the young
plant, but has usually quite disappeared in the adult.

The typical bundle of the Monocotyledons is amphivasal
concentric. Such a bundle is shown in Fig. 113, HH. In this
type of bundle the tracheary tissue surrounds the phloem, and
not the phloem the tracheary tissue, as is generally the case in
the Pteridophyta. The amphivasal concentric bundle is char-
acteristic of the Monocotyledons from the grasses (Zizania,
ete.) to the orchids (J/abenaria, Cypripedium, ete.), and is
quite as constant a feature as the scattering disposition of the
fibrovascular strands. This type of bundle resembles the am-
phicribral concentric bundles of the Pteridophytes in showing
no evidence of secondary growth. Amphivasal strands are ab-
sent in the leaves and reproductive axes of the Monocotyledons,
and generally in the seedlings as well. Unlike the concentric
strands of the Gymnosperms, they are accordingly a cenogenetic
and not an ancestral feature, but on account of their widespread
occurrence in the group have an important phylogenetic signifi-
cance.

Secondary growth has been supposed to be entirely lacking
in the collateral strands of the Monocotyledons, but Queva 1”
has recently shown that characteristic secondary growth is
present in the bundles of the tuberous base of the stem of
the liliaceous genus Gloriosa. The activity of the cambinm
becomes apparent during the season after the formation of the
tuber, when it is passing its reserve products into the aerial
stem. From the oceurrence of a cambium in Gloriosa, ete.,
Qneva hag drawn the conclusion that the Monocotyledons are
derived from the lower Dicotyledons.

The most salient anatomical features of the Monocotyledons
are the scattering disposition of their closed fibrovascular
strands, and the presence of amphivasal concentric bundles.
These features, although practically universal, are not primi-
tive; for a study of the leaves, reproductive axes, and seedlings
shows often a dicotyledonous disposition of the generally col-
lateral strands. Hence we may infer that the Monocotyledons

316 MORPHOLOGY OF ANGIOSPERMS

are a strictly monophyletic and modern group, since they possess
in common a very characteristic mode of arrangement of bun-
dles of a unique type, and since neither the structure of the
bundles nor their mode of disposition is palingenetic. Further,
the evidence of secondary growth in Gloriosa, ete., would seem
to indieate that the Monocotyledons have come off somewhere
from the Dicotyledons, which they resemble so closely in their
essential reproductive organs. This view of the matter seems
strengthened by the greater reduction of the sporogenous tissue
in the megasporangium of the Monocotyledons as compared
with the lower Dicotyledons, and by the entire absence of the
probably primitive phenomenon of chalazogamy, which is so
characteristic of the lower Dicotyledons. In the present state
of our knowledge we are apparently justified in considering
the Monocotyledons to be a modern, strictly monophyletic and
specialized group, derived from the Dicotyledons or their parent
stock, possibly by adaptation in the first instance to an amphibi-
ous mode of life.*

LITERATURE CITED

. Merrenius, G. H. Beitriige zur Anatomie der Cycadeen. 1857.

. Renavtt, B. Cours de Botanique Fossile. Paris. 1880-1884.

. STRASBURGER, E. Histologische Beitriige. III. 1891.

4. TrpGHEM, P. vAN. Traité de Botanique. Paris. 1891.

5. CAMPBELL, D. H. Mosses and Ferns. New York. 1895.

6. WILLIAMSON and Scott. Further Observations on the Organiza-
tion of the Fossil Plants of the Coal-measures. Part. 3. Lygi-
nodendron and Heterangium. Phil. Trans. Roy. Soc. London
B. 186: 1896.

7. Scorr, D. H. The Anatomical Characters presented by the Ped-
uncle of the Cycadaceae. Annals of Botany 11: 399-419. pls.
20-21, 1897.

8. WorsDELL, W. C. On Transfusion Tissue; its Origin and Func-
tion in the Leaves of Gymnospermous Plants. Trans. Linn.
Soe. London Bot. II. 5: 301-319. pls. 23-26. 1897.

. Porontk, H. Metamorphose der Pflanzen im Lichte Palaeontolo-
gischer Thatsachen. Berlin. 1898.

10. Jerrrey, E. C. The Development, Structure, and Affinities of the

Genus Equisetum. Mem. Boston Soc. Nat. Hist. 5: 155-190.

pls. 26-30, 1899.

wnwr

Jo}

* Tt should be noted that the manuscript of Chapters XVI and XVII was
completed April 1, 1902.

B, stem of Adéantum pedatum. C,
DP, voung stem of same; £) stem of Selaginella laevigata 5

Fic. 108.— 4, part of stem of Gleichenia flabellata;

rhizome of Pteris aquilina ;
F. central cylinder of Osmunda Claytoniana.

H, central cylinder of

Fie, 109.—4, forking central eylinder of Osmunda einnamomeas
7, same, showing presence of internal phloem: J, part of central eylinder
stem ot J/ete-

sume |
shown in Z more highly magnified; AY mesarch bundle of same; Z,
vy central mass of primary woody .c2, see ondary

,

rangium Gricvii, after Scorry x A.
cortex: pel

wood: ie, inner cortex; @t, leaf trace; 7, adventitious root; oc, outer

petiole,

Fie. 110,—J/, diagrammatic transverse section of stem of Medullosa anglica, after Scorr:
st, concentric strands ; pd, periderm ; 7f, leaf trace; V, diagram of part of transverse
section of stem of Medullosa Solmsi, after Weber and Srerze., from Poronim: pla,
pli, larger concentri¢ strands ; st, smaller concentric strands; QO, transverse section
of stem of Lyyinodendron Oldhamium, after WitiiAMson and Seorr; P, part of

woody zone of same; Y, same, showing internal secondary wood and internal
phloem.

Wieearereas
esas tees

Fic. 111.—F, stem of Zamia floridanay S, central eylinder of same; 7, cortical foliar
bundle of Cyeas revolutay 7) petiolar bundle of same, Vy) seetion of part of leat ofa
speeies of Cordattes ; HW, cotyledonary bundle of Ginkgo biloba: pry protoxylem }
wy, centripetal woods 2, centrifugal wood,

Fie. 112.—.\, cotyledonary bundle of Cephalotarus drupacea: pa, protoxylem; 1, cen-
tripetal wood; 7%, centrifugal wood; ¢/, transfusion tissue ; J, longitudinal section
of cotyledonary bundle of Cephalotarus Fortunei: ph, phloem ; other lettering as in
V: Z small branch of Zhuja occidentalis; AA, root of Pinus Strobus; BB, part of

sae,

Fra. 113.—CC, wood of Guefum Gnemon; DD, stem of Ranunenulus acris, EE, bundle
of same; /7) acrial stem of Smilae herbacea, GG, part of subterranean stem of
Clintonia borealis; M7, mupblivasal concentric bundle of the subterranean stem of
Smilae herbacea.

COMPARATIVE ANATOMY OF ANGIOSPERMS BLT

. Potonié, H. Pflanzenpalaeontologie. Berlin. 1899.
. QUEVA, C. Contributions & l’'anatomie des Monocotyledonées. I.

Les Uvulariées tubereuses. Lille. 1899.

. JEFFREY, E.C. The Morphology of the Central Cylinder in the

Angiosperms. Trans. Canadian Inst. pp. 40. pls. 7-11. 1900.

. Scott, D. H. Trans. British Assn. Ady. Sci. 1900.

Studies in Fossil Botany. London. 1900.

. WORSDELL, W. C. The Comparative Anatomy of Certain Species

of Encephalartos. Trans. Linn. Soc. London Bot. II. 5: 445-
459, pl. 43. 1900.
Trans. British Assn. Ady. Sci. 1900.

. Faut., J.H. The Anatomy of the Osmundaceae. Bot. Gazette

82: 381-420. pls. 14-17. 1901.

9, JEFFREY, EK. C. The Structure and Development of the Stem in

the Pteridophyta and Gymnosperms. Phil. Trans. Roy. Soc.
London B. 195: 119-146. pls. 6. 1902.

LITERATURE CITED

Anprews, F. M. Development of the Embryo-sac of Jeffersonia
diphylla. Bot. Gazette 20: 423-424. pl. 28. 1895.

ATKINSON, G. F. Studies on Reduction in Plants. Bot. Gazette 28:
1-26. pls. 1-6. 1899.

On the Homologies and Probable Origin of the Embryo-sac.
Science 13: 530-588. 1901.

Batrour, I. B. The Angiosperms. Address to the Botanical Section,
Brit. Assn. Adv. Sei. Glasgow. 1901.

Baricka-Iwanowska, G. P. Contribution 4 létude du sac embryon-
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INDEX

[The italicized numbers refer to figures. ]

Acacia, §

Acantha e, 176, 177, 256, 269.

Acer, 134, 136, 147; rubrum, 52.

Aceraceae, 20, 97, 104, 110, 248, 278.

Achariaceae, 249.

Aconitum Napellus, 82, 99, 100, 111,
125, 221.

Acorus, 275.

Acrogamy, 150.

Actinomorphy, 15, 16.

Adiantum pedatum, 297, 303, Fig.
108.

Adoxa, 277.

Adoxaceae, 259.

Aesculus, 147.

Agave, 25; americana, 34.

Aglaonema, 192.

Agraphis, 63, 77, 84, 86; nutans, 84.

Agrimonia, 58.

Aizoaceae, 244.

Alchemilla, 87, 93, 96, 104, 151, 211,

218, 219; acutangula, 212; alpes-
tris, 212; alpina, 55, 58, 59, 79, 82,

212; arvensis, 150, 211, 212; “hy-
brida,” 212; pastoralis, 212, 221;
pubescens, 212; sericata, 93, 212,
221; speciosa, 212.

Alisma, 77, 136, 138, 151, 152, 195,
196; type of embryo, 188; Plan-
tago, 188.

Alismaceae, 77, 97, 167, 171, 229,
230, 263, 265.
Allium, 64, 77; canadense. 218;

Cepa, 81; cernuum, 218; fistulo-
sum, 81, 218; odorum, 103, 217,
218, 221; tricoccum, 218; ursi-
num, 81, 218.
Alnus, 60, 131, 132,
tinosa, 30, 147.

149, 150; glu-

Aloe, 53.

Alopecurus pratensis, 98.

Alsineae, 131.

Alstroemeria, 81; psittacea, 81.

Alternation of generations, 288.

Althaea, 39.

Alyssum, 63, 65, 199.

Amarantaceae, 46, 244.

Amarantus retroflexus, 21.

Amaryllidaceae, 157, 178, 236,
264, 266.

Amentaceae, 241.

Amentiferae, 60, 62, 100, 105, 112,
113, 241.

Amici, 143, 145.

Amsonia, 103.

Amygdalus, 199, 208.

Anacardiaceae, 248.

Anagallis, 25; arvensis, 46.

Anatomy of Angiosperms, 311; of
Dicotyledons, 311; of Gymno-
sperms, 296; of Monocotyledons,
314.

Ancistrocladaceae, 249.

Andrews, F. M., 64, 76, 84, 101.

Androecium, 23.

Anemarrhena, 209, 281.

Anemone, 64; nemorosa, 156,
159; patens Nuttalliana, 157.

Anemonella, 100; thalictroides, 60.

Angiosperms,. comparative anatomy
of, 311; contrasted with Gymno-
sperms, 1; embryogeny of, 2; fos-
sil. 272; gametophyte of. 3; geo-
evaphie distribution of. 261;
phylogenetic relation to Gymno-
sperms, 283, to Pteridophytes,
284; phylogeny of, 280; sporo-
phyte of, 2.

238,

158,

333

B34 MORPHOLOGY

Anoda, 101.

Anona, 131.

Anonaceae, 245.

Antennaria, 101; alpina, 80, 82, 92,
95, 166, 170, 211, 212; dioica, 80,
82, 166, 211.

Anther, 23; dehiscence of, 41.

Anthericum, 77.

Antherozoids, 160.

Anthyllis tetraphyla, 203.

Antipodal cells, 94, 98, 111.

Aphyllon uniflorum, 80, 170, 206.

Aplectrum hiemale, 194.

Apocynaceae, 255, 269.

Aponogetonaceae, 229, 263, 266.

Aquifohaceae, ¢

Aquilegia, 64, 78: canadensis, 99.

Araceae, 10, 41, 48, 56, 77, 98, 103,
174, 192, 233, 263, 266, 274, 275.

Arachis hypogaea, 203.

Arales, 233, 263, 275, 287.

Aralia, 277, 278; racemosa,

Araliaceae, 65, 79, 85, 251.

Araucarioxylon, 307

ote

Archangelica, 136.

Archesporium of megasporangium,
57; of microsporangium, 32.

Archichlamydeae, 97; classification
of, 240; geographic distribution
of, 266,

Arctostaphylos,
ursi, 42.

Avil, 53.

Arisaema, 62, 77, 103.

Aristolochia, 277.

Aristolochiaceae, 176, 244.

Avistolochiales, 244.

Armeria, 103: vulgaris, 172.

Arum, 146, 147, 233.

Arundina, 156,

Arundinites, 275.

Arundo, 275.

Asarwm, 101.

Ascherson, P., 196.

Asclepiadaceae, 30, 38, 41, 61, 135
157, 255, 269.

Asclepias, 37, 55, 74, 102, 109, 122,
124, 127, 133; 135, .146, 167, 169;
Cornuti, 82, 102, 127, 157, 159,
167; Syriaea, 123
85, 127.

Asparagus officinalis, 125.

Asperula, 82, 202;

alpina, 42; Uva-

lo

tuberosa, 82,

azurea, 202.

ANGIOSPERMS

Asphodelus, 53.

Aster novae-angliae, 100, 101.

Astilbe, 19, 37, 39, 59, 87, 103, 108;
japonica, 58.

Astrapaea, 131.

Astrocarpus, 51.

Atkinson, G. F., 75, 81.

Avena, 80, 136; fatua, 33, 63,
192.

Avicennia, 199; officinalis. 80.

Azalea indica, 125, 129.

78, 98,

Baillon, H. E., 42.

Balanophora, 50, 95, 166; dioica, 47;
elongata, 49, 92, 218, 2:0, 221;
globosa, 48, 49, 92, 218; indica,
49, 92; polyandra,, 47, 49.

Balanophoraceae, 30, 48, 55, 64, 65,
19, 92, 170, 176, 201, 206, 243.

Balanopsidaceae, 242.

Balanopsidales, 242.

Balfour, I. B., 209.

Balicka-Iwanowska, G. P., 96, 102,
103, 106, 107.

Balsaminaceae, 248,

Bambusa,. 275.

3arber, C. A., 22.

Barnes, C. R., 24, 103, 104. 131, 186,
146, 148.

Barringtonia Vriesei, 201.

Bartonia, 50.

Basellaceae, 244.

Basigamy, 150.
3atidaceae, 244,

Begonia, 125, 129.

Begoniaceae, 249.

Belajeff, W., 129, 131, 188.

Bennettitales, anatomy of, 306.

Benson, Margaret, 59, 66, 87, 100,
105, 147, 148, 149, 151.
3entham, G., 227.

Berberidaceae, 64, 245, 278, 282.

Berberis, 41.

Bernard, C. H., 61, 79, 86, 91, 92
95, 108, 154, 166, 218.

Bessey, (G3. E., B83,

Betula, 60, 149, 150;

Betulaceae, 243, 278.

Bignoniaceae, 97, 176, 177, 256.

Billings, F. H., .95, 103, 106, 107,
111, 113, 148, 149, 200, 201.

Bixaceae, 249.

Blattiaceae, 250,

alba, 147.

INDEX 385
3ombacaceae, 249. 192, 195, 196, 200, 242, 282, 285,

Borraginaceae, 131, 256, 269, 271.

Borraginales, 258.

Borago, 7.

Boveri, Th., 18

Bower, F. O.,

Brasenia, 51.

Braun, <A., 208, 213,

Bromeliaceae, 9, 264, 266,

Brongniart, A., 143, 227.

Brown, Robert, 143.

Brunelliaceae, 246.

sruniaceae, 246.

Bryophyllum, 51.

Budding, 210.

Burmannia javanica, 213.

Burmanniaceae, 206, 238, 266.

sums, G. P., 103, 106, 107, 113,
170.

surseraceae, 247.

Butomaceae, 229, 263, 266, ¢

Butomus, 25, 50, 63, 75, 77, ¢

Suxaceae, 248,

3yblis, 108; gigantea, 107.

Byxbee, Edith, 129.

wo

221, 227.

pa

Cabomba, 51.

Cactaceae, 79, 97, 108, 147, 151, 250,
268, 312.

Caesalpinia, 247; mimosoides, 203.

Calamus, 233.

Calandrinia compressa, 42.

Calanthe veratrifolia, 30, 39.

Caleeolaria, Pavonii, 42.

Caldwell, O. W., 30, 37, 39, 40, 63, 77,
92, 108, 136, 167, 193.

Calendula, 103; lusitanica, 95, 111.

Calla, 233; palustris, 42.

Callipeltis cucullaria, 5:

Callitrichaceae, 247.

Callothamnus, 23.

Caltha, 64, 78, 137,
60, 99, 152, 156, 17.

Calycanthaceae, 245, 267.

Calyceraceae, 259, 270.

Camassia Fraseri, 138.

Campanales , 270.

Campanula, 25, 95, 103, 104, 131,
136, 146; americana, 148.

Campanulaceae, 102, 106, 110, 176,
259, 270.

Campbell, D. H., 27, 28, 48, 63, 77,
78, 84, 89, 90, 98, 99, 133, 135, 154,

101.

157; palustris,
?
Oo.

287, F

‘andolleaceae, 259, 270.

Canellaceae, 249.

anna, 110, 179; indica, 64, 73, 81,
105, 171, 1733 limbata, 244:

Sannabineae, 56, 148, 150.

‘annaceae, 64, 171, 237, 264, 266.

vannon, W. A., 33, 63, 78, 80, 98,
136, 192.

‘apparidaceae, 57, 246.

‘aprifoliaceae, 259, 269,

Japsella, 18, 61, 65, 94, 157, 196, 199;
type of embryo, 199: Bursa-pas-
toris, 16, 19, 187, 197, 198, 293;
Heegeri, 293.

Carboniferous Monocotyledons, 273.

Carex acuta, 74, 124, 128.

Caricaceae, 249,

(

(

Carlson, G. W. F., 293.

‘arpel, 24; morphology of, 22.

Carpinus, 60, 66, 87, 110, 131, 148,
150; Betulus, 105, 147.

Carum bulbocastanum, 206,

Carya, 148; olivaeformis, 149.

Caryocaraceae, 249.

Caryophyllaceae, 57, 97, 103, 179,
244, 267.

Cassia lentiva, 42.

Castanea, 60, 102,
garis, 100, 105.

Casuarina, 28, 59, 60, 66, 79, 87, 92,
101, 102, 105, 109, 149, 150, 157,
167, 312; suberosa, 149.

Casuarinaceae, 97, 242.

Casuarinales, 242.

Celakovsky, L. F., 8, 9, 52, 288.

Celastraceae, 248.

Celastrales, 248.

Celastrus, 53.

Centrolepidaceae, 235, 264, 276.

Centrosomes, 153.

Centrospermae, 244.

Centrospermales, 244.

Cephalotaceae, 246.

Cephalotaxus, drupacea, 308.
112: Fortunei, 308, Fig. 112.

Ceratophyllaceae, 157, 176, 245, 267,
282.

Ceratophyllum, 177, 208; demersum,
157, 201; submersum, 82, 177.

Cercis, 203; siliquastrum, 203.

Chalazogamy, 149.

109, 110; vul-

Fig.

B56

Chambe foe os all cg ra 31, 52, 58,
60, Ff, 19, Bly Bf, or , LOO, 101,
132; ie. ‘134, 135, on 138, 151,
199.

Chauveaud, G. L., 55, 123, 217, 221.

Cheiranthus Cheiri, 221.
Chenopodiaceae, 57, 103, 179, 244.
Chlaenaceae, 249.

Chloranthaceae, 242.
Chlorophytum Sternbergianum, $1.

Chodat, R., 79, 91, 92, 95, 103, 166,
218.

Chromatin, behavior during fusion,
153.

Chromosomes, 128, 211; reduction
of, 80, 128.

Chrysanthemum, 38; Leucanthe-
mun, 61.

Cicer arietinum, 204.

Cistaceae. 56, 249.

Citrus, 147, 214; Auyrantium, 213,
27).

Cladosiphonic, 298.

Clematis, 64, 84, 99, 122, 156; cir-

rhosa. GO.
Clethraceae, 253.

Clintonia borealis, 314, Fig. 113.
Clusia alba, 221.

Cneoraceae, 247.

Cnicus, 157; arvensis, 17.
Coalescence, 12.

Cochlospermaceae, 249.
Coelebogyne, 214; ilicifolia, 213, 221.
Coffea arabica, 221.

Colchicum autumnale, 147.
Columelliaceae, 256.

Combretaceae, 250.

Commelina, 77, 99; stricta, 63.

Commelhnaceae, 56, 63, 196, 235, 264,
206.

Compositae, 12, 15, 16, 18, 22, 24,
33, 46, 58, 61, 87, 95, 97, 100, 101,
102), 108; LII;, 03; Ve, Ler; 4;
259, 270, 271.

Conard, H. 8., 201, 207.

Conducting tissue, 25.

Coniterales, 286; anatomy of, 308.

Connaraceae, 246.
Conrad, A. H., 31, 34,
94, 147.
Contortae 5.
Convallaria, 63, 64, 77,
majalis, 33, 81;

58, 60, 66, 79,

133;
multiflora,

136;
125s

MORPHOLOGY OF ANGIOSPERMS

Convolvulaceae, 131, 269.
Conyza, 96, 101.

Cook, M. T., 176.
Corallorhiza multiflora,
Cordaitales, anatomy of,
Cordaites, Fig. 111.
Coriariaceae, 248.

Corn, xenia, 180.
Cornaceae, 251.
Cornucopiae, 63, 98.
Cornus, 147; sanguinea, 125.
Correns, C., 180.

Corry,. T.. H.,. 132.

Corydalis, cava, 172, 173, 206; lutea,
206; nobilis, 206.
Corylus, 60, 87, 132,
americana, 30, 31;

147.
Corynocarpaceae, 248.
Coryphanthe, 231.
Costus, 77, 171.
Cotyledon, phylogeny of,

gle in Dicotyledons, 206;

Dicotyledons, 208.

195.
307.

148, 149,
Avellana,

150;
105,

208; sin-
three in

Coulter, J. M., 36, 37, 38, 60, 61, 65,
81, 87, 88, 131, 135, 136, 151, 169,
170, 193, 199, 290.

Crassulaceae, 246.

199.
Dicotyledons, 276, 278;

Crataegus,
Cretaceous

Monocotyledons. 273.
Crinum, 53; capense, 178.
Crocus, 94, 99, 104, 146, 147.
Croomia, 266; japonica, 266; pauci-
flora, 266.
Crossosomataceae, 246.
Crucianella, 82. 85; macrostachya,
SO.
Cruciferae, 18, 57, 65, 97, 157, 246,
267.
Cueurbita, 150, 151, 179, 205.
Cucurbitaceae, 131, 174, 259, 270.
Cunoniaceae, 246.

Cuphea, 68, 96, 104,

Cupuliferae, 97, 131, 174, 313.

Cuseuta, 174, 206.

Cyeadales, 286; anatomy of, 304.

Cyeadofilices, 109; anatomy — of,
300.

Cyeads, 301.

Cyeas, 305; revoluta, 305, Fig. 111.

Cyclamen, europaeum, 42; persicum,
206,

INDEX

Cyclanthaceae, 232, 263, 266, 275.

Cyclanthera, 28,

Cyclic series, 12, 228, 234.

Cydonia, 59.

Cymbalaria, 158.

Cynanchum, 55, 124.

Cynocrambaceae, 244.

Cynomoriaceae, 250.

Cynomoriwn, 76, 147, 201.

Cyperaceae, 122, 230, 265, 275.

Cypripedium, 132, 238, 239, 315; bar-
batum, 81; spectabile, 133.

Cyrillaceae, 248.

Cyrtosperma, 263.

Cystisus, 203; Laburnum, 203.

Cytinaceae, 206.

Dadoxylon, 307.
Damascena, 158.
Datiscaceae, 249.

Datura, 38, 157,
J51, 165, 178.

De Candolle, A. P., 9, 227.

Definitive nucleus. See Endosperm
nucleus.

De Jussieu, A. L., 227.

Delphinium, 64, 76, 78, 84, 87; ela-
tum, 156; exaltatum, 100; tri-
corne, 60, 87, 99, 154.

Delpino, F., 282.

De Vries, H., 180, 292, 293.

Diapensiaceae, 253, 269.

Dichapetalaceae, 247.

Dicotyledons, 4, 11; anatomy of,
311; cyclic number of, 5; embryo

158; laevis, 136,

of, 4, 7, 196; fossil, 276; leaves
of, 5, 6; in Lower Cretaceous,

276; in Tertiary, 278; in Upper
Cretaceous, 278; phylogeny of,
281; prophyllum of, 7; roots of,
7; seed germination, 6; vascular
bundles of, 4.

Dieffenbachia, 77, 84, 192.

Digitalis, 136.

Dilleniaceae, 249.

Diodia, 104, 111; virginiana, 102.

Dioecism, 20, 21.

Dioscoreaceae, 196, 236,
274, 276.

Dipsaceae, 18, 102, 269.

Dipterocarpaceae, 249.

Dodel, A., 217, 221.

Doronicum, 101; macrophyllum, 32.

264, 266,

lad
37

[w%)

Double fertilization, 155, 156, 160,
180; nature of, 182.

Draba verna, 293.

Dracaena, 237, 285.

Droseraceae, 246.

Ducamp, L., 65, 74, 79, 85.

Duggar, B. M., 31, 37, 136.

Dumée et Malinvaud, 58, 64.

Dunn, Louise B., 100.

Ebenaceae, 254.

Ebenales, 254, 269.

Egg, 93, 145; apparatus, 93; rest of,
169.

Ehrarta panicea, 98.

Eichhornia, 80, 94, 95, 135, 136; eras-
sipes, 73, 81, 135, 170.

Kichler, A. W., 8, 15, 51, 52, 227, 241.

Elaeagnaceae, 250.

Klaeocarpaceae, 249.

Elatinaceae, 249.

Elatine hexandra, 125.

Elmore, C. J., 218.

Elodea, 157, 170.

Elfving, F., 124, 132, 148.

Embryo, 187; Alisma type, 188; An-
giosperms and Gymnosperms con-
trasted, 2; Capsella type, 199;
degree of development, 205; de-
partures from type. 195; Lilium
type, 193; Monocotyledons and
Dicotyledons contrasted, 4, 7; of
Dicotyledons, 196; of Monocoty-
ledons, 188; Orchid type, 194;
origin of, 144; Pistia type, 192.

Embryo-sac, chambered, 175, 176;
enlargement of, 103, 109; number
of, 86; nutritive jacket, 103, 109;
nutritive mechanism, 108.

Embryonal vesicle, 143.

Empetraceae, 248.

Enantioblastae, 236.

Endlicher, 8. L., 52, 227.

Endosperm, 165; continuation of
growth, 178; displaced by em-

bryo, 174; division of, 169; feeble
development of, 171; function of,
179; morphological character of,
181; nature of, 183; nature of tis-
sue, 178; nuclear fusions, 172;
nucleus, 89, 166; origin by free
nuclear division, 172; origin by
wall-formation, 174.

B35 MORPHOLOGY

Endothecium, 34.
ae nee nutans, 156,
; LOS 1128

93 , 240,

Epacridacene 253, 269,

piensa, 53.

yny, ld.

Hpilobium, 122.

Epipactis, 194:

Equisetum, 306:

Evianthis, 99, 281

Kricaceae,

Ericales,

Erigeron, 151, 156,
delphicus, 169.

Eriobotrya, 59, 85

he dare 56,

Ernst, 39, 90,
219, 2 -

Evodium, 103.

Ervum Erviha, 204.

Evythraea Centaureum, 42.

Erythrina cristagalhi, 204.

Erythronium, 25, 53, 64, 77, 135,
136, 146, 151, 193, 215; albidun,
215; americanum, 81, 214, 222;
dens-canis, 222.

Erythroxylaceae, 247.

Eucalyptus. 277, 278.

Eucryphiaceae, 249.

Euonymus, 53; americanus, 221; lat-
ifolius, 213.

Euphorbia, 94. 136, 151: corollata,
33, 49, 74, 126, 129; dulcis, 217;
Lathyrus, 125.

Euphorbiaceae, 63, 97, 247.

Exarch, 300.

Exine, 131.

palustris, 193.
telemateia, 154.
; hiemalis, 206.

, 253.
Pi:
158, 169;

phila-
» 96, 101.

, 264, 266, 276.
160, 193, 215,

Fagaceae, 2

Fagales, 2 :

Fagus, 59, 87, 110, 147, 151;
ica, 105, 147.

Familler, L., 8.

Famintzin, A., 188, 196.

Farinales, 235, 264, 276.

Farinosae, 235.

Fatsia japonica,

Faull, J. H., 299.

Female gametophyte, 71;
ment of, 87; tetrad, 71;
larities in, 91; nuclei, 153.

Ferraris, T., 94, 99, 104.

sylvat-

~~)

4.

develop-
irregu-

OF ANGIOSPERMS

Fertilization, 143; double, 155, 156,
160, 180, 182; generative and vege-
tative, 159.

Ficaria ranunculoides,

Ficus, 131; hirta, 212.

Filicales, 286.

Filiform apparatus, 94.

Fischer, A., 55, 58, 61, 64, 7, 92,
OS.

Flacourtiaceae, ¢

Flagellariaceae,

Floral leaves, origin of, 9.

Flower, 8; bisporangiate, 21; “ co-
alescence,’ 12; definition of, 9;
~ dioecious,” 20; hypogyny to epig-
yny, 13; morphology of members,
22; naked to differentiated calyx
and corolla, 10; organogeny, 16;
primitive vs. reduced, 10; spiral to
cyclic, 11; symmetry, 15.

Focke, W. O., 179.

Fol, H., 154.

Forsythia, 103.

Fossil angiosperms, 272.

Fouquieraceae, 249.

Fourcroya, 131.

Povilla, 132.

Fragaria, 199.

Frank, A. B., 309.

Frankeniaceae, 249,

Frititaria, 77; imperialis, 81;
leagris, 81, 156;
nella, 156.

Frye, T. C., 37; 39, 55, 61, 5
92, B02, 106, 122, 124, 197, oy
135, 157, 159, 167, 169.

Fuchsia, 63, 125.

Fullmer, E. L., 33, 74, 126, 135.

Fumaria, 246,

Funkia, 64, 77, 215;

OL}, 22)
Fusion, behavior of chromatin dur-
3 sexual nuelei, 153;

125, 129.

Me-
persica, 123; te-

ovata, 125, 213,
Sieboldiana, 81.

ing, 153; of
triple, 158,

Fusion nucleus, 166; division of,
169.
Gager, C. &., 124.

Galanthus nivalis, 42.

Galega orientalis, 204.
Galeopsis angustifolia, 42.
Galieae, 97, 102, 104, 111, 113.
Galium, 108.

INDEX 389

Galtonia, 77; candieans, 81, 82.

Gametophyte, 42; Angiosperms and
Gyimnosperms contrasted, 2; te-
male, 71; male, 121.

W. F., 14, 214, 221.

Garcinia, 42.

Ganong,

Gaura, 30.
Geissolomaceae, 250.
Generative,
182; nucleus, 132,
135,
Gentiana, 50.
Gentianaceae,

fertilization,
division — of,

cell, 133;

Geraniaceae, 20, 131, 247.
Geraniales, 247.
Geranium, 200.
Gesneraceae, 256, 269.
Gein, 55, 199.

Giltay, E., 179.

Ginkgo, 307; biloba, Fig. 111.

Ginkgoales, anatomy of, 307.

Gladiolus, 99, 104.

Glaucium luteum, 221.

Gleichenia, 302; flabellata, 300, Fig.
108.

Globularia, 103, 176; cordifolia, 42,
107.

Globulariaceae, 256,

Gloriosa, 315.

Glumales, 230, 231, 264, 275.

Glume, 231.

Gluniflorae, 230.

Gnetales, anatomy of, 310.

Gnetum, 88, 90, 91, 283, 284, 285,
286, 310; Gnemon, 310, Fig. 173.
Goebel, C., 8, 9, 15, 20, 21, 28, 30,
33, 34, 43, 64, 122, 131, 133, 147,

196, 206, 221.
Goldflus, Mlle. M., 111.
Golinski, St. J., 136, 137.
Gomortegaceae, 245.
Gomphrena, 91, 92.
Gonyanthes candida, 170, 213.
Gonystylaceae, 249.
Goodeniaceae, 259, 270.

269.

57, 63, 77, 98, 104, 109,
112, 115, 157, 174, 205, 230, 265,

20D:

Gray, A., 8.
Grebel, Dr.,

213.

Grubbiaceae,

Guignard, L., 30, 33, 38, 39, 59, 60,
61, 62, 63, 64, 65, 71, 77, 80, 81,
82, 84, 85, 86, 87, 89, 90, 94, 95,
96, 97, 98, 99, 101, 104, 105, 122,
33, 136, 147, 151, 153, 154,
156, 157, 158, 159, 165, 169,
172, 178, 180, 202, 203, 204,
Zify Q2L;

Gunnera, 89, 90, 166, 313.

Guttiferae, 249.

Gynmadenia, 77, 92, 94, 95; conop-
sea, 64, 82, 148, 194, 217, 221.

Gymmnosperms, comparative anato-
my of, 296; contrasted with An-
giosperms, 1; embryogeny of, 2:
gametophyte of, 3: sporophyte
of, :2. :

Gynoecium, 24.

Gynostemium, 238.

Habenaria, 315; blephariglottis, 195;
tridentata, 195,

Haemodoraceae, 236, 264, 266.

Hall, J. G., 63, 77, 92, 95, 146, 167,
71, 17S, 192, 215, 216, 222.

Hallier, H.,

Haloraghidaceae, 250, 312.

Halsted, B. D., 136.

Hamamelidaceae, 246.

Hamamelis, 30, 41: virginiana, 147.

Hanausek, T. F., 221.

Hanstein, J., 188, 196, 198.

Hartig, Theodore, 145.

Hartog, M., 288.

Haustoria, 104, 109, 202.

Hautschicht, 95.

Hebenstreitia, 177.

Heckeria, 79, 90, 101, 167, 170, 178,
179, 201.

Hedysarum coronarium, 203.

Hegelmaier, F., 102, 178, 192,
207, 217, 218,221.

Heleocharis palustris, 728.

Helianthemum, 61, 122.

Helianthus annuus, 155, 156.

Heliconia, 171.

Helleborus, 64. 84; cupreus, 60; foet-
idus, 82, 156.

Helobiales, 171, 229, 231, 234, 263,
275, 287.

Helosis, 79, 95, 103, 166; guayanen-
sis, 91, 92, 218.

206,

340

Hemerocallis, 64,
fulva, 33, 74, 125,
Hepatica, 30, 38, 53,

Hernandiaceae, 245.

Hesperis, 136.

Heterangium, 300, 301, 302; Grievii,
300, Fig. 109.

Hibiseus, 156,

Hicoria, 148.

Hill, T. G., 99, 192.

Himantoglossum, 156; hireinum, 82.

Hippeastrum aulicum, 148.

Hippocastanaceae, 248.

Hippocrateaceae, 248.

Hippuris, 55, 64.

Hofmeister, W., 18, 32, 47, 48, 49,
51, 53, 71, 94, 101, 106, 125, 132,
143, 146, 147, 148, 176, 178, 181,
206, 221, 222.

Holferty, G. M., 63, 76,
176, 192.

Holm, Theodore, 282.

Homalomena, 263.

Hooker, J. D., 227.

Houstonia, 55, 202.

D’Hubert, i., 79, 108, 147, 151.

Humiriaceae, 247.

Humphrey, J. E., 64,
TW, Lis, 192.

Hyacinthus orientalis, 74,

Hydnoraceae, 244.

Hydrocaryaceae, 250.

Hydrocharitaceae, 157, 171, 229, 230,
263, 265, 275.

Hydrophylaceae, 176, 256, 269.

Hydrostachyaceae, 246.

Hypericum, 24; calycinum, 18.

Hypogyny, 13, 14.

Hypophysis, 188, 198.

77, 78, 96,

77, 104, 154,

Teacinaceae, 248.

Ikeda, T., 77, 96, 99, 104, 111, 112,
1538, 157, 158, 174.

Impatiens, 131, 205,

Integument, 53.

Intine, 13).

Iridaceae, 64, 236, 264, 265, 276.

Iris, 77, 99, 155; sibirica, 217, 221;
squalens, SL; stylosa, 64.

Irmisch, 'P., 206.

Isobilaterality, 16.

Isoetaceae, 285.

Tsoetes, 196, 284, 285, 287.

MORPHOLOGY OF ANGIOSPERMS

Jasminum, 95.

Jeffersonia, 64, 76, 84; diphylla, 101.

Jeffrey, E. C., 214, 215, 222, 281,
296, 297, 298, 300, 301, 303, 304,
305, 308, 309, 311, 312.

Johnson, D. 8., 79, 89, 90, 101, 104,
105, 186,..137, 158, 166, 167, 168,
170, 176, 178, 179, 200, 201, 242.

Johnson, T., 47, 55.

Jonsson, B., 221.

Jordan, K. F., 293.

Juel, H. O., 73, 74, 76, 80, 82, 92,
101, 124, 126, 128, 129, 147, 166,
170, 201, 211.

Juglandaceae, 46, 157, 243, 278, 284.

Juglandales, 243, 268.

Juglans, 91, 146, 147, 148, 150, 156,
157, 158; cinerea, 149: cordifor-
mis, 60, 79, 84, 87; nigra. 92, 96;
regia, 90, 149. ;

Juneaceae, 236, 264, 265, 276.

Juneaginaceae, 196, 229, 230, 263,
265, 275.

Juncagineae, 171.

Juneus, 121.

Jurassic Monocotyledons, 273.
Justicia, 131.

Kamienski, F., 206.
Karsten, G., 60, 79, 84, 87.
96, 157, 158, 284.
Kauffmann, N., 28.
Kerner, A., 42.
Klebs, G., 288, 289.
Koch, L., 80, 206.
Ioeberliniaceae, 249.
Kolliker, A., 292.
Kornicke, F., 180.
Koernicke, M., 63, 81, 137.
Kkorschinsky, 8., 292.

91, 92,

Labiatae, 16, 24, 104, 106, 176, 256,
269, 271.

Labiatales, 258.

Lacistemaceae, 242.

Lactoridaceae, 245.

Land, W. J. G., 29, 82, 151, 155,
156, 160, 169, Figs. 35 and 36.

Lang, F. X., 107, 108.

Lang, W. H., 288, 289.

Lappa, 122.

Lardizabalaceae, 245, 267.

Larix europaea, 154.

INDEX

Lathyrus, 136; heterophyllus, 204;
odoratus, 204.

Lauraceae, 245, 267.

Laurus, 277.

Lawson, A. A., 129.

Leaves, Monocotyledons and Dicot-
yledons contrasted, 5, 6.

Leavitt, R. G., 193, 194.

Lecythidaceae, 250.

Leeuwenhoek, A., 213.

Leguminosae, 15, 16, 20, 55, 65, 97,
174, 202, 246, 267, 279; embryos
of, 202.

Leguminosites, 277.

Leitneriaceae, 242.

Leitneriales, 242.

Lemna, 10, 30, 39, 63, 77, 92, 95,
103, 136, 167,193; reduced flowers,
10; minor, 37, 40.

Lemnaceae, 233, 234, 263, 265.

Le Monnier, G., 181, 182.

Lennoaceae, 253,

Lentibulariaceae, 256.

Lepidium, 157.

Leptosiphon, 103.

Leucojum vernum, S1.

Lilaea, 28, 46, 99; subulata, 27, 47,
196, 285.

Liliaceae, 64, 76, 82, 97, 103, 109,
157, 174, 1938, 209, 236, 264, 265,
274, 276.

Liliales, 236, 264, 276.

Liliiflorae, 236.

Lilium, 25, 41, 58, 64, 73, 77, 80;
81, 84, 95, 97, 104, 123, 134, 135,
136, 137, 146, 151, 157, 159, 161,
169, 193, 195; type of embryo,
193; auratum, 134, 138; candi-
dum, 61, 81, 86, 130, 131, 153, 154;
croceum, 81; Martagon, 81, 1<2,
130, 154, 156, 158, 221; philadel-
phicum, 29, 54, 61, 81, Pigs. 35
and 36, 88, 135, 157, 160, 193;
pyrenaicum, 156; tigrinum, 16, 81,
134, 135, 157.

Limnanthaceae, 248.

Limnocharis, 63, 77, 92, 95, 167, 171,
175, 176, 192; emarginata, 146,
2155216. 222:

Linaceae, 247.

Linum, 103.

Liriodendron, 277, 278.

Listera, 194; ovata, 82, 193, 194.

d41

Lloyd, F. E., 55, 58, 61, 80, 82, 88,
86, 97, 101, 102, 104, 108, 202.

Loasaceae, 176, 249.

Lobelia, 80, 103, 111.

Lobeliaceae, 24, 30, 48, 58, 106, 110.

Loganiaceae, 255, 269.

Longo, B., 150.

Lonicera, 80; coerulea, 125.

Loranthaceae, 55, 65, 97,
176, 243.

Loranthus, 50, 61, 85, 86, 91, 92,
97, 177; europaeus, 221, pentan-
drus, 49, 200; sphaerocarpus, 43,
50, 199, 200.

Lotsy, J. P., 28, 34, 48, 49, 50, 51,
79, 92, 186, 166, 218.

Luerssen, C., 131.

Lupinus, 202, 204; luteus, 205; mu-
tabilis, 205; poly-
phyllus, 205; 2009 5
truncatus, 205.

Lychnis, 21.

Lyciun, 80.

Lycopodiales, 286.

Lyginodendron, 301, 302, 303,
306; Oldhamium, 301, 302,
110; robustum, 302.

Lygodium, 300.

Lyon, F. M., 49,
129, 136, 151.

Lyon, H. L., 169, 201, 207, 208, 282.

Lysichiton, 63, 192; kamtschatcense,
98, 192.

Lythraceae, 104, 110, 250.

104, 110,

pilosus, 205;
subcarmnosus,

305,
Pig.

74, 94, 100. 126,

Magnolia, 277.

Magnoliaceae, 245.

Magnus, P., 28.

Mahonia indica, 64.

Maize, xenia, 180.

Male cells, 136; not concerned in
fertilization, 161.

Male gametophyte, 121.

Male nucleus, 136, 152, 157, 166;
change in size and form, 152;

fusion, 153; its part in fertiliza-
tion, 160; movements of, 157: ver-
miform, 161.

Malesherbiaceae, 249.

Malpighi, M., 143.

Malpighiaceae, 247.

Malva, 38.

Malvaceae, 33, 131, 157, 249.

345

bo

Malvales. 249, 267.

Mangifera indica, 221.

Marantaceae, 171, 237

Marattiaceae, 301.

Maregraviaceae, 249.

Marié¢, M., 312.

Martyniaceae, 256.

Massula, 39.

Mayacaceae, 235, 264, 266.

Medicago, 104; falcata, 204.

Medinilla, 42.

Medullosa, 301, 302; anglica, 301,
Fig. 110; Solmsi, 301, Fig. 110;
stellata, 301.

Megasporangium, 46; archesporium
of, 57; cauline, 46; mother-cell,
66; parietal cells, 62; time of de-
velopment, 52.

Megaspore, 71; germination of, 87;
number of, 76; the functional, 84.

Melastomataceae, 250, 268.

Meliaceae, 247.

Mehanthaceae, 248.

Melissa officinalis, 42.

Mellink, J. F. A., 71, 84.

Menispermaceae, 245,

Menispermites, 277.

Mentha, 38; aquatica, 32, 33.

Menyanthes, 103; trifoliata, 32.

Merrell, W. D., 34, 35, 82, 101, 103,
136, 137, 151, 158, 199.

Mertensia, 136.

Mesembrianthemum, 63.

Metamorphosis, 8, 10, 22.

Mettenius, G. H., 304, 305.

Microspermae, 238,

Microsporangium, 27; archespori-

cauline, development

mother-cells, 38; number
parietal layers, 34: tape-
tim, 36; time of formation, 30.

Microspores, 121; germination of,
132; number of, 125; wall of,
181.

Mimosa, 203, 247, 267, 268, 279;
Denhartii, 216, 221.

Mimoseae, 30, 33, 132.

Mirbel, C. F., 56.

Mohl, TH. von, 145.

Monimiaceae, 245.

Monocotyledons, 4, 11; anatomy of,
3l4; classification of, 227; eyclic
number of, 5; embryo of, 4, 7,

264, 266.

um, 32;
of, 32%
of, 29;

MORPHOLOGY OF

ANGIOSPERMS

188; fossil, 272; in Carboniferous,
; In Cretaceous, 273; in Juras-

sic, 273; in Tertiary, 275; geo-
graphic distribution of, 262; leaves

of, 5, 6; phylogeny of, 281; pro-

phyllum of, 7; roots of, 7; seed
germination, 6; vascular bundles
of, 4.

Monotropa, 148, 158, 206; Hypopi-

tys, 145, 156; uniflora, 96, 102,
147, 153, 157, 159, 167.

Monotropaceae, 176.

Moraceae, 243, 278.

Moringaceae, 246.

Morus albus, 221.

Mother-cell, of megasporangia, 38;
of microsporangia, 38.

Mottier, D. M., ; 60; G61; 62; 76,
17, 18; 82; 84, 87, 94, 99, 101, 103,
124, 129, 130, 134, 136, 146, 153,
154, as 199

Murbeck, 58, 59,
93, 96, ns 150, 175, 196, 311, 212,
218, 219, 221, 285

Musaceae, 171, 237, 264, 266, 276.

Muscari neglectum, 81.

Mutation theory, 292.

AMyoporaceae, )

Myoporum, 103, 200; serratum, 201.

Myosurus, 64, 99.

Myrica, 277.

Myricaceae, 242.

Myricales, 242.

Myristica, 53.

Myristicaceae, 245.

Myrothamnaceae, 246.

Myrsinaceae, 254, 269.

Sea dat easaa 277.

Myrtaceae, 201, 250, 268.

Myrtales, 250.

Muyzodendraceae, 243.

Myzodendron, 105, 110;
tum, 47, 55.

punctula-

Niigeli, C., 32.

Naiadaceae, 97, 157, 171,
263, 265.

Naias, 28, 41, 46,133,171, 192;

27; major, 81, 157, 165,
2oT:

229, 230,

flexilis,
170, 216,

77, 99, 156.
90, 146,

Narcissus,
Nawaschin, &.,
155, 156, 180.

148, 149, 150,

INDEX 3438

Nelumbo, 169, 201, 207, 208.

Némec, B., 74, 75.

Nemophila, 136, 176.

Neottia, 131, 133; nidus-avis, 82, 122;
ovata, 38, 39.

Nepenthaceae, 246, 268.

Nicotiana, 80, 96, 97, 157, 158; Taba-
cum, 136, 147, 151, 158.

Nigella, 99, 151, 158; damascena,
157, 159; sativa, 156.

Nolanaceae, 256, 269.

Nothoscordon fragrans, 213, 221.

Nuphar, 50, 176; lutea, 208.

Nyctaginaceae, 96, 97, 244.

Nyctandra, 42.

Nymphaea, 9, 22, 23, 50, 53, 176,
201, 207; alba, 82.

Nymphaeaceae, 103, 110, 176,
282, 312, 313.

Obolaria, 50.

Ochnaceae, 249.

Oenothera, 104; Lamarckiana, 292;
lata, 293.

Olacageae, 243.

Oleaceae, 97, 255.

Oliniaceae, 250,

Oliver, F. W., 55, 80, 85, 95, 106,
109, 111, 134, 148, 169, 177, 178,
199.

Onagraceae, 30, 97, 131, 250, 267.

Onobrychis petraea, 204.

Ononis, alopecuroides, 204; fruti-
cosa, 204.

Opiliaceae, 243.

Opuntia, tortispina, 214; vulgaris,

214, 221.

Opuntiales, 250.

Orange, 213.

Orchid, 195; type of embryo, 194.

Orchidaceae, 15, 30, 58, 64, 97, 103,
113, 132, 136, 147, 157, 171, 194,
206, 234, 238, 266.

Orchidales, 238, 264, 276.

Orchis, 51, 77, 145, 156; latifolia,
144, 145; maculata, 33, 38, 39,
144; mascula, 82, 121, 126; Morio,
144, 145, 221; pallens, 64.

Organogeny of flower, 16.

Ornithogahun, 64, 97, 99;
91; pyrenaicum, 61.

Orobanchaceae, 176, 206, 256, 269.

Orobanche, 80.

23

nutans,

Orobus angustifolius, 65, 204; au-
reus, 204.

Osmunda, 302, 303; cinnamomea,
298, 299, Fig. 109; Claytoniana,
298, Fig. 108; regalis, 299.

Osterwalder, A., 99, 100, 111, 221.

Osyris, 105.

Ovary, 24, 26.

Overton, E., 71, 221.

Overton, J. B., 63, 64, 81, 82, 94,
100, 170, 199, 212.

Ovulary, 24.

Ovules, foliar, 50; morphological
nature of, 51; development of, 53;
forms of, 56.

Oxalidaceae, 247.

Paeonia spectabilis, 82.

Palet, 221;

Palmaceae, 231, 262, 266, 274, 275.

Palmales, 231, 262, 275.

Pandanaceae, 228, 262, 266, 273, 275.

Pandanales, 228, 231, 262, 275.

Papaver, 136; orientale, 65.

Papaveraceae, 65, 246.

Papilio, 247, 267.

Parietales, 249.

Paris quadrifolia, 159, 160.

Parthenogenesis, 210.

Passiflora, 131.

Passifloraceae, 249.

Payer, J. B., 16, 20.

Péchoutre, F., 59, 199.

Pedaliaceae, 97, 106, 110, 176, 177,
256, 269.

Pedicularis, 106.

Penaeaceae, 250.

Pentaphyllaceae, 248.

Peperomia, 79, 88, 90, 136, 137, 153,
178, 179, 200; pellucida, 89, 166,
168, 178, 200, 242, 284.

Pepo macrocarpus, 143.

Perigyny, 13, 14.

Perisperm, 103; function of, 179.

Peristylis grandis, 194.

Personales, 15, 24, 258.

Petasites, 101.

Petit-Thouars, 213.

Peucedanites, 277.

Pfeffer, W., 19.

Pfitzer, E., 194.

Phajus, 156.

Phalaenopsis grandiflora, 194.

o44

Phaseolus, 179, 208; miultiflorus,
204.
Philydraceae, 235, 264.
Phlox Drummondii, 113.
Phyllocactus, 108.
Phragmites, ;
Phrymaceae, 256,
Phylloglossum, 300.
Phyllosiphonic, 208.
Phylogeny of Angiosperms, 280.
Phytelephas, 178, 231, 262.
Phytolacca, 179.
Phytolaccaceae, 103, 179, 244.
Pinguicula vulgaris, 42.
Pinus, 160; Strobus, 112, 309.
Piper, 79, 90, 167, 178; medium, 168.
Piperaceae, 46, 56, 79, 103, 178, 179,
201, 242.
Piperales, 242
Pirolaceae, 253.
Pirotta, R., 150.
Pirus Malus, 1
Pistia, 178, 192, 195, 201, 263, 275;
type of embryo, 192.
Pistil, 25.
Pisum sativum, 204.
Pittosporaceae, 246.
Placenta, 25.
Plantaginaceae, 102,
271.
Plantaginales, 258, 269.
Plantago, 269; lanceolata, 107.
Platanaceae, 246.
Plumbaginaceae, 254.
Poacites, 275.
Podophyllun, 53, 282, 313;
tum, 31, 82, 124.
Podostemonaceae, 246.
Polar nuclei, 92; fusion of, 95.
e, 103, 256, 269.

106, 176, 258

)

pelta-

Polemoniace:

Polemoniales, 258.

Pollen mother-cell, division of, 126.

Pollen-tube, 143; branching of, 148;
development of, 146; discharge of,
152; entrance into sae, 151; in
cleistogamous flowers, 146; Prop-
fen, 148; time between pollination
and fertilization, 146.

Pollination, relation to endosperm,
169.

Pollinium, 132.

Polyembryony, 213.

Polygalaceae, 104, 110, 247.

MORPHOLOGY OF ANGIOSPERMS

Polygonaceae, 46, 56, 179, 244, 267.

Polygonales, 244.

Polygonum, 94; divaricatum, 94.

Polypompholyx, 108.

Polystelic, 297.

Pontederia, 104, 146, 151;
Sl.

Pontederiaceae,
97, 235, 264, 26%

Populus, 52, 133, 277, 278; monilif-
era, 30, 31; primaeva, 276; trem-
uloides, 60.

Portulaca, 143.

Portulacaceae, 244.

Potamogeton, 63, 76, 77, 96
136, 176, 192; natans,
sus, 33, 62, 78.

Potamogetonaceae, 229, 230, 234
263, 265, 274, 275.

Potentilla, 18.

Pothos longifolia, 148.

Potonié, H., 300, 303, 308, Fig. 110.

Prantl, K., 8, 56.

Primula farinosa, 312.

Primulaceae, 19, 103, 254,

Primulales, 254, 269.

Principes, 231.

Pringsheim, N.,

Proangiosperms,

Proembryo, 188.

Propfen, 148.

Prophyllum, Monocotyledons and Di-
cotyledons contrasted, 7.

Proteaceae, 131, 243, 268, 278.

Proteales, 243.

Proteophyllum, 277.

Protocorm, 209,

Protolemna, 275.

Protostelic, 297.

Prunus Cerasus, 125.

Pseudo-monocotyledons, 206,

Pseudo-polyembryony, 2:

Psilotum triquetrum, 75

Pteridophytes, anatomy of, 296.

Pteris aquilina, 297, 298, 301, 303,
Fig. 108.

Punicaceae, 250,

Purkinje, J.

Pyrethrum, 85, 87;
G1.

Pyrola rotundifolia, 4
206; uniflora, 42.

Pyrolaceae, 176,

cordata,

269.

281, 283, 286.

pbalsaminatum,

ras)

secunda,

INDEX 845

Quercus, 34, 66, 79, 94, 147, 148, 208;
Robur, 147; velutina, 31, 58, 60,
147.

Queva, C., 5

Quiinaceae, %

Rafflesiaceae, 244,

Ramondia pyrenaica, 42.

Ranales, 245, 287.

Ranunculaceae, 21, 60, 64, 78, 84, 99,
102, 111, 153, 157, 158, 169, 245,
267, 282, 312.

Ranunculus, 11, 16, 36, 37, 51, 55, 64,
73, ST, 100, 131, 186, 151, 158, 170,
199, 311, 312; flowers of, 11, 16;
abortivus, 60; acris, 312, 313, Fig.
113; Cymbalaria, 157; Ficaria,
206, 207, 282; Flammula, 156;
multifidus, 65, 88; septentrionalis,
61.

Rapateaceae, 235, 264.

Ray, John, 227.

Reichenbach, H. G., 132.

Renault, B., 308.

Reseda, 20, 156; odorata, 173.

Resedaceae, 57, 157, 246.

Restiaceae, 56.

Restionaceae, 235, 264, 276.

Reversion, 22.

Rhamnaceae, 249,

Rhamnales, 249.

Rhinanthus, 106.

Rhizophoraceae, 250.

Rhododendron, 132.

Rhoedales, 246.

Rhopalocnemis, 79, 92, 136;
loides, 28, 34, 49, 57.

Ricinus, 24, 179.

Riddle, Lumina C., 63, 65, 199.

Robinia, 147.

Rohrbach, P., 28.

Romulea, 94, 99, 104.

Root, Monocotyledons and Dicoty-
ledons contrasted, 7.
Rosa, 18, 84, 87, 221, 247;

eels

Rosaceae, 59, 60, 62, 63, 87, 199, 246,
267, 279.

Rosales, 246.

Rosanoff, §., 33, 152.

Rose, J. N., 135, 136.

tosenberg, O., 36, 37, 74, 77, 81,
124.

phal-

livida, 58,

122

ah,

tubiaceae, 18, 58, 61, 80, 97, 102,
111, 118, 202, 259, 269.

Rubiales, 259, 269.

Rubus, 18, 59.

Rudbeckia speciosa, 156.

Rumex, 21; Patientia, 125.

Ruppia, 196, 285; rostellata, 175.

Ruta, 97; graveolens, 62.

Rutaceae, 20, 247.

Sabiaceae, 248.

Sachs, J., 15.

Sagittaria, 96, 104, 135, 136, 137, 169,
175, 176; variabilis, 152, 154, 175,
188, 189, 191.

Salicaceae, 97, 242.

Salicales, 242.

Salix, 52, 60, 87, 94, 136, 151, 199,
277, 278; glaucophylla, 30, 58, 79,
95; petiolaris, 28,

Salvadoraceae, 255, 269.

Salvia, 95, 97; pratensis, 85.

Sambucus, 136.

Sanguisorba, 58.

Santalaceae, 55, 105, 110, 176, :

Santalales, 243.

Santalum, 91, 94, 105; album, 221.

Sapindaceae, 20, 248.

Sapindales, 248.

Sarcodes, 25, 80, 97,
199; sanguinea, 148.

Sargant, Ethel, 73, 81, 82, 157, 182,
207, 209, 281, 282.

Sarraceniaceae, 246] 268.

Sarraceniales, 246.

Sassafras, 41, 277.

Saururaceae, 97, 104, 109, 176, 242.

134, 169, 178,

Saururus, 79, 104, 110, 176, 179;
cernuus, 104, 105.

Saxifraga caespitosa. 125.

Saxifragaceae, 59, 97, 246, 267.

caevola, 103.

Schacht, H., 55, 94, 131,
145, 221.

Schaffner, J. H., 28, 38, 53, 63, 74,
T7,- 81, 88, 96, 121, 126, 135, 135,
136, 137, 188, 146; 151,. 152, 153,
154, 169, 175, 188,189, 191, 193,
215.

Schleiden, M. J., 9, 52, 55, 144, 145.

Schlotterbeck, M., 106.

Sehmid. B., 206.

Schnege, H., 89, 90, 166.

143, 144,

346

Schniewind-Thies, J., 77, 81, 84.

Schrankia uncinata, 221.

Schwere, 8., 102, 199,216, 221.

Scilla, 64, 84, 156; non-scripta, 81;
sibiriea, 81.

Scitaminales, 237, 264, 276.

Scitamineae, 57, 64, 77, 97, 103, 104,
109, 171, 192, 237.

Serophularia nodosa, 16, 125.

Serophulariaceae, 96, 97, 103, 106,
110, 176, 256, 269, 271.

Seleranthus annuus, 125.

Scott, D. H., 288, 300, 301, 302, 303,
304, 305, 306, 307, Fig. 110.

Scytopetalaceae, 249.

Sedum, 51.

Seed, Monocotyledons and Dicotyie-
dons contrasted, 6,

Nelaginaceae, 176, 177.

Selaginella, 285, 287; laegivata, Fig.
108.

Senecio, 87, 101, 169, 199.

Seward, A. C., 273, 302; aureus, 61.

Sherardia arvensis, 101.

Shibata, K., 96, 102, 147, 148, 153,
157, 189, 167,

Shoemaker, D. N., 30, 147.

Sibbaldia procumbens, 42.

Silene, 94.

Silphium, 34, 101, 103, 136, 137, 151,
156, 158, 160, 199; integrifolium,
35, 82; laciniatum, 82, 155.

Simarubaceae, 247.

Sinningia Lindleyana, 221.

Siphonostelic, 297.

Sium, 65, 94, 96, 103, 199; cicutae-
folium, 79.

Sisyrinchium, 77; ‘ridifolium, 64.

Smilax, 274; herbacea, Fig. 113.

Smith, Amelia C., 80, 170, 206.

Smith, Arma, 30.

Smith, R. W., 34, 37, 63, 73, 77, 7
80, 81, 94, 95, 135, 136, 146, 15
170.

Snow, Laetitia M., 160.

8
1;

Solanum, 41; Lycopersicum, 42.
Solms-Laubach, H., 196, 206, 295
Sonneratiaceae, 250.

Sparganiaceae, 98, 228, 262, 265, 275.
Sparganium, 112, 138, 192, 228, 229,

233; simplex, 47, 98, 135.

Spartium junceum, 203.

MORPHOLOGY OF ANGIOSPERMS

Spathe, 232.

Spathiflorae, 233.

Spergularia rubra, 46.

Spermacoceae, 202.

Spermatozoids, 136, 160.

Sperms, 136, 160.

Spiral series, 11, 228.

Spiranthes, 193.

Sporangia, foliar and cauline, 27, 46;
in winter, 30; periblem origin of,
27, 46.

Sporophyte, 41; Angiosperms and
Gymnosperms contrasted, 2.

Stachyuraceae, 249.

Stackhousiaceae, 248.

Stamen, 23; morphology of, 22.

Staminodia, 24.

Stangeria paradoxa, 305.

Staphylea, 136, 145; pinnata, 172.

Staphyleaceae, 248, 278.

Stellaria, glauca, 125; Holostea, 84.

Stemona, 266.

Stemonaceae, 236, 264, 266.

Sterculiaceae, 249.

Sterzel, J. T., Fig. 110.

Stevens, W. C., 124.

Stichneuron, 266.

Stigma, 25.

Strasburger, E., 38,
64, 71, 73, 74, , 82, 8
92, 94, 99, 104, 121, 122, 123, 124
126, 128, 138, 145,
146, 148, 154, 157, 158, 159, 171,
L723 li8y its USL, 182s, 183,201;
202, 208, 213, 214, 215, 217, 221,
284, 294, 313.

Strelitzia, 171.

Strobilus, theory of, 288.

Sueccisa pratensis, 293.

Suspensor, 113, 190, 192,
202.

Stylidaceae, 103, 106, 108, 110, 170.

Styhdium squamellosum, 107, 113.

Styracaceae, 254.

Sympetalae, 97;
252;
268.

Sympetaly, 13.

Symphytum officinale, 125.

Symplocaceae, 254.

Symplocarpus, 31, 37, 136; foetidus,
315.

Synanthae, 232.

193, 194,

classification of,
geographic distribution of,

INDEX

Synanthales, 232, 263, 275.

Synapsis, 126.

Synearpy, 13.

Synergids, 91, 94; as an haustorium,
111; disorganization of, 151.

Syringa, persica, 125; vulgaris, 125.

Taccaceae, 236, 264, 266.

Tamaricaceae, 249.

Tangl, E., 125.

Tapetum, 36.

Taraxacum, 101, 102, 157, 199; offi-
cinale, 216, 221.

Tertiary, Dicotyledons, 278;
cotyledons, 275.

Tetrads, 71, 121, 126.

Tetragonolobus purpureus, 203.

Thalia dealbata, 171.

Thalictrum, 63, 64, 78, 94, 199; dio-
icum, 100; Fendleri, 212; purpu-
rascens, 100, 170, 212.

Theaceae, 249.

Theobroma Cacao, 42.

Thesium, 61, 105.

Thomas, Ethel M., 137,
157, 158.

Thuja occidentalis, 309, Fig. 112.

Thunbergia, 131.

Thymelaeaceae, 250, 268.

Tiliaceae, 249.

Tischler, G., 172.

Todea barbara, 299.

Torenia, 111, 136; asiatica, 104, 106.

Tovariaceae, 246.

Tozzia alpina, 42.

Tracheid-like cells in nucellus, 100,
109.

Tradescantia, 81, 135, 136; virginica,
63.

Trapa, 171, 205; natans, 206.

Trapella, 55, 80, 85, 95, 106, 110, 111,
177, 199; sinensis, 85.

Tremandiaceae, 247.

Tretjakow, S., 217, 218, 221.

Treub, M., 49, 50, 59, 61, 64, 66, 71,

Mono-

152, 156,

79, 80, 84, 85, 87, 91, 92, 149, 166,

167, 170, 193, 194, 199, 200, 201,
212; 213; 218, 221.

Treviranus, 213.

Tricyrtis, 64, 77, 96, 99, 104, 158,
174; hirta, 77, 111, 772, 153, 157.

Trifolium, pratense, 221; resupina-
tum, 203.

B47

Triglochin, 63, 192; maritima, 99.

Trigoniaceae, 247.

Trillium, 30, 64, 77, 86, 89; grandi-
florum, 81, 90, 159; recurvatum,
52, 72, 81.

Triple fusion, 158, 160, 166; nature
of, 182.

Triplochitonaceae, 249.

Triticum, 63, 136, 137;

Tritonia, 77.

Triuridaceae, 229, 263, 266.

Triuridales, 229.

Trochodendraceae, 245.

Tropaeolaceae, 247.

Tropaeolum, 39, 171, 207.

Trophophylls, 282.

Tschirch, A., 106.

Tschistiakoff, I., 125.

Tube nucleus, 133;
of, 135.

Tubiflorae, 256.

Tubiflorales, 256, 269.

Tulasne, L. R., 106.

Tulipa, 77, 89, 156, 193; Celsiana,
156; Gesneriana, 81, 215, 219, 222;
sylvestris, 90, 156.

Tumboa, 310.

Turneraceae, 249.

Tussilago, 101.

Typha, 28, 38, 63, 74, 77, 104, 121,
131, 133, 229, 233; latifolia, 28,
126.

Typhaceae, 97, 228, 262, 265, 275.

vulgare, 81.

fragmentation

Ulmaceae, 243.
Ulnus, 147, 148, 150, 151;' montana,
150; pedunculata, 150.
Umbellales, 251.
Umbelliferae, 15, 16, 55,
251, 267.
Umbelliflorae, 2/
Unger, D. F., 55.
Urticaceae, 56,
Urticales, 243.
Utricularia, 206.
Utriculariaceae, 106.
Uvularia, 84.

Vacciniaceae, 176, 177.

Vaccinium, 80; Oxycoccus, 42; ulig-
inosum, 42.

Vaillantia, 104, 111; hispida, 102,
202.

348 MORPHOLOGY

Valerianaceae, 18, 259, 269.
Van Tieghem, Ph., 30, 49,
297, 298, 309.

Vascular bundles, Monocotyledons
and Dicotyledons contrasted, 4.
Vegetative, apogamy, 210; fertiliza-

tion, 182; nucleus, 132.
Velloziaceae, 236, 264, 266.
Verbenaceae, 80, 176, 177, 256, 269.
Verticillatae, 242.
Vesque, J. 63, 63, 71, Tis

Sb.

Viburnum, 277, 278.
Vicia narbonnensis,
Vinea, 136.
Vincetoxicum,

rum, 217, 221.
Viola, 25.
Violaceae, 249.
Viscum, 61, 97, 176, 206;

221; articulatum, 79, 87.
Vitaceae, 249.

Viticella, 156.
Vochysiaceae, 247.

52, 92,

80, 84, 85,

204.

medium, 221; nig-

album,

Ward, H. Marshall, 58, 61, 63, 7
76, 77, 80, 87, 92, 94, 148, 194.

Warming, E., 28, 32, 33, 51, 52, 53,
flee
Webb, J. E., 19, 37, 39, 58, 59, 87,
108.
THE

OF ANGIOSPERMS

Webber, H. J., 180, 181.
Weber, M., Fig. 110.
Westermaier, M., 98, 99, 111.

Wiegand, K. M., 33, 62, 63, 64, 73,
Ths (8; 8150 138,, 136; 192:
Walle; (N.; 121, °128,; 124, -125;. 126;

129, 196.
Williamson, W., 301, 302, Fig. 110.
Wimmel, Th., 125.
Wolffia, 234.
Worsdell, W. C., 303, 306,
Wroylie, R. B., 157, 170.

308, 309.

Xenia, 179.

Xyridaceae, 56, 235, 264, 266.
Yueea, 63,
84.

64, 77, 285; gloriosa,

Zamia, 305, 307;
LUT,
Zannichellia, 27, 28. 46, 51, 192, 196,
285; palustris, 195.
Zea, 94, 98, 153, 157, 158, 172, 179.
Zingiberaceae, 171, 237, 264, 266.
Zinger, N., 56, 148, 150.
Zizania, 315.
Zostera, 37, 74, 77,
81, 124.
Zygomorphy, 15, 16.
Zygophyllaceae, 20, 247.

floridana, 304, Fig.

122 .

eae.

marina, 36,

(1)

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